Similar articles

Abstract: Atypical sensory responsivity is widely reported in autistic individuals and is related to elevated functional difficulties. Dynamically, altered initial responses and/or habituation rates could underlie their atypical averaged responses to repeated sensory stimuli. In this study we aimed to measure the arousal level in response to different types of auditory stimuli and the dynamic change of atypical arousal level using pupillometry in autistic children. In Experiment 1, 43 autistic children and 49 neurotypical (NT) children were asked to passively listen to a mild sound and an aversive sound repeatedly. In Experiment 2, 39 autistic children and 44 NT children who went through Experiment 1 listened to a gradually emerging non-startling sound and a suddenly emerging startling sound in a random order. We found that the autistic group showed hyper-arousal in response to the aversive sound and the startling sound as reflected by their larger change in pupil area. In comparison, these autistic children demonstrated normal arousal in response to the mild sound and the non-startling sound. Dynamically, the autistic group had a larger peak pupil area change than the NT group in the first trial and a normal habituation rate to the aversive sound. In summary, our results suggest hyper-arousal to aversive and startling stimuli and the role of larger initial responses in hyper-arousal in autism. Minimizing aversive and startling sensory stimuli or gradually increasing the volume of aversive auditory stimuli to allow autistic children to adapt using the principle of habituation is recommended to reduce the arousal level and problematic behaviors of autistic children.

瞳孔测量揭示孤独症儿童对听觉刺激的过高唤醒反应

[1]American Psychiatric Association, 2013. Diagnostic and Statistical Manual of Mental Disorders, 5th Ed. American Psychiatric Association Publishing, Washington, USA.

[2]BaranekGT, DavidFJ, PoeMD, et al., 2006. Sensory experiences questionnaire: discriminating sensory features in young children with autism, developmental delays, and typical development. J Child Psychol Psychiatry, 47(6):591-601.

[3]BarryRJ, JamesAL, 1988. Coding of stimulus parameters in autistic, retarded, and normal children: evidence for a two-factor theory of autism. Int J Psychophysiol, 6(2):139-149.

[4]Ben-SassonA, CermakSA, OrsmondGI, et al., 2008. Sensory clusters of toddlers with autism spectrum disorders: differences in affective symptoms. J Child Psychol Psychiatry, 49(8):817-825.

[5]Ben-SassonA, HenL, FlussR, et al., 2009. A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. J Autism Dev Disord, 39(1):1-11.

[6]BradleyMM, MiccoliL, EscrigMA, et al., 2008. The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45(4):602-607.

[7]CascioCJ, Moana-FilhoEJ, GuestS, et al., 2012. Perceptual and neural response to affective tactile texture stimulation in adults with autism spectrum disorders. Autism Res, 5(4):231-244.

[8]ChangMC, ParhamLD, BlancheEI, et al., 2012. Autonomic and behavioral responses of children with autism to auditory stimuli. Am J Occup Ther, 66(5):567-576.

[9]ChiuTA, AnagnostouE, BrianJ, et al., 2016. Specificity of autonomic arousal to anxiety in children with autism spectrum disorder. Autism Res, 9(4):491-501.

[10]ConzelmannA, GerdesABM, MuchaRF, et al., 2014. Autonomic hypoactivity in boys with attention-deficit/hyperactivity disorder and the influence of methylphenidate. World J Biol Psychiatry, 15(1):56-65.

[11]DawsonME, SchellAM, FilionDL, 2016. The electrodermal system. In: Cacioppo JT, Tassinary LG, Berntson GG (Eds.), Handbook of Psychophysiology, 4th Ed. Cambridge University Press, Cambridge, UK, p.217-243.

[12]de VriesL, FouquaetI, BoetsB, et al., 2021. Autism spectrum disorder and pupillometry: a systematic review and meta-analysis. Neurosci Biobehav Rev, 120:479-508.

[13]EspinosaL, Lundin KlebergJ, HofvanderB, et al., 2020. Enhanced social learning of threat in adults with autism. Mol Autism, 11:71.

[14]EzellJ, HoganA, WillEA, et al., 2022. Cardiac startle response and clinical outcomes in preschool children with fragile X syndrome and autism spectrum disorder. Front Psychiatry, 12:729127.

[15]GandhiTK, TsouridesK, SinghalN, et al., 2021. Autonomic and electrophysiological evidence for reduced auditory habituation in autism. J Autism Dev Disord, 51(7):2218-2228.

[16]GeisslerJ, RomanosM, HegerlU, et al., 2014. Hyperactivity and sensation seeking as autoregulatory attempts to stabilize brain arousal in ADHD and mania?Atten Defic Hyperact Disord, 6(3):159-173.

[17]GhaniU, SignalN, NiaziIK, et al., 2020. A novel approach to validate the efficacy of single task ERP paradigms to measure cognitive workload. Int J Psychophysiol, 158:9-15.

[18]GreenSA, Ben-SassonA, 2010. Anxiety disorders and sensory over-responsivity in children with autism spectrum disorders: is there a causal relationship?J Autism Dev Disord, 40(12):1495-1504.

[19]GreenSA, Ben-SassonA, SotoTW, et al., 2012. Anxiety and sensory over-responsivity in toddlers with autism spectrum disorders: bidirectional effects across time. J Autism Dev Disord, 42(6):1112-1119.

[20]GreenSA, RudieJD, ColichNL, et al., 2013. Overreactive brain responses to sensory stimuli in youth with autism spectrum disorders. J Am Acad Child Adolesc Psychiatry, 52(11):1158-1172.

[21]GreenSA, HernandezL, TottenhamN, et al., 2015. Neurobiology of sensory overresponsivity in youth with autism spectrum disorders. JAMA Psychiatry, 72(8):778-786.

[22]GreenSA, HernandezL, LawrenceKE, et al., 2019. Distinct patterns of neural habituation and generalization in children and adolescents with autism with low and high sensory overresponsivity. Am J Psychiatry, 176(12):1010-1020.

[23]HaesenB, BoetsB, WagemansJ, 2011. A review of behavioural and electrophysiological studies on auditory processing and speech perception in autism spectrum disorders. Res Autism Spectr Disord, 5(2):701-714.

[24]HalekohU, HøjsgaardS, YanJ, 2006. The R package geepack for Generalized Estimating Equations. J Stat Softw, 15(2):1-11.

[25]HodgsonAR, FreestonMH, HoneyE, et al., 2017. Facing the unknown: intolerance of uncertainty in children with autism spectrum disorder. J Appl Res Intellect Disabil, 30(2):336-344.

[26]Hoehn-SaricR, McLeodDR, 2000. Anxiety and arousal: physiological changes and their perception. J Affect Disord, 61(3):217-224.

[27]HoeksB, LeveltWJM, 1993. Pupillary dilation as a measure of attention: a quantitative system analysis. Behav Res Methods Instrum Comput, 25(1):16-26.

[28]JamalW, CardinauxA, HaskinsAJ, et al., 2021. Reduced sensory habituation in autism and its correlation with behavioral measures. J Autism Dev Disord, 51(9):3153-3164.

[29]JamesAL, BarryRJ, 1984. Cardiovascular and electrodermal responses to simple stimuli in autistic, retarded and normal children. Int J Psychophysiol, 1(2):179-193.

[30]JonesRSP, QuigneyC, HuwsJC, 2003. First-hand accounts of sensory perceptual experiences in autism: a qualitative analysis. J Intellect Dev Disabil, 28(2):112-121.

[31]JoshiS, LiY, KalwaniRM, et al., 2016. Relationships between pupil diameter and neuronal activity in the locus coeruleus, colliculi, and cingulate cortex. Neuron, 89(1):221-234.

[32]JungJ, ZbozinekTD, CummingsKK, et al., 2021. Associations between physiological and neural measures of sensory reactivity in youth with autism. J Child Psychol Psychiatry, 62(10):1183-1194.

[33]KhalfaS, BruneauN, RogéB, et al., 2004. Increased perception of loudness in autism. Hear Res, 198(1-2):87-92.

[34]KlebergJL, FrickMA, BrockiKC, 2021. Increased pupil dilation to happy faces in children with hyperactive/impulsive symptoms of ADHD. Dev Psychopathol, 33(3):767-777.

[35]KlebergJL, FrickMA, BrockiKC, 2023. Eye-movement indices of arousal predict ADHD and comorbid externalizing symptoms over a 2-year period. Sci Rep, 13:4767.

[36]KuiperMWM, VerhoevenEWM, GeurtsHM, 2019. Stop making noise!Auditory sensitivity in adults with an autism spectrum disorder diagnosis: physiological habituation and subjective detection thresholds. J Autism Dev Disord, 49(5):2116-2128.

[37]LaneAE, MolloyCA, BishopSL, 2014. Classification of children with autism spectrum disorder by sensory subtype: a case for sensory-based phenotypes. Autism Res, 7(3):322-333.

[38]MarcoEJ, HinkleyLBN, HillSS, et al., 2011. Sensory processing in autism: a review of neurophysiologic findings. Pediatr Res, 69(5 Part 2):48R-54R.

[39]MarkramK, MarkramH, 2010. The Intense World Theory ‒ a unifying theory of the neurobiology of autism. Front Hum Neurosci, 4:224.

[40]McCormickC, HesslD, MacariSL, et al., 2014. Electrodermal and behavioral responses of children with autism spectrum disorders to sensory and repetitive stimuli. Autism Res, 7(4):468-480.

[41]McDiarmidTA, BernardosAC, RankinCH, 2017. Habituation is altered in neuropsychiatric disorders—a comprehensive review with recommendations for experimental design and analysis. Neurosci Biobehav Rev, 80:286-305.

[42]MillerLJ, AnzaloneME, LaneSJ, et al., 2007. Concept evolution in sensory integration: a proposed nosology for diagnosis. Am J Occup Ther, 61(2):135-140.

[43]NuskeHJ, VivantiG, DissanayakeC, 2014. Reactivity to fearful expressions of familiar and unfamiliar people in children with autism: an eye-tracking pupillometry study. J Neurodev Disord, 6:14.

[44]O'ConnorK, 2012. Auditory processing in autism spectrum disorder: a review. Neurosci Biobehav Rev, 36(2):836-854.

[45]OrekhovaEV, StroganovaTA, ProkofyevAO, et al., 2008. Sensory gating in young children with autism: relation to age, IQ, and EEG gamma oscillations. Neurosci Lett, 434(2):218-223.

[46]PalkovitzRJ, WiesenfeldAR, 1980. Differential autonomic responses of autistic and normal children. J Autism Dev Disord, 10(3):347-360.

[47]PfeifferB, KinnealeyM, ReedC, et al., 2005. Sensory modulation and affective disorders in children and adolescents with Asperger’s disorder. Am J Occup Ther, 59(3):335-345.

[48]RobertsonAE, SimmonsDR, 2015. The sensory experiences of adults with autism spectrum disorder: a qualitative analysis. Perception, 44(5):569-586.

[49]RudlingM, NyströmP, BölteS, et al., 2022. Larger pupil dilation to nonsocial sounds in infants with subsequent autism diagnosis. J Child Psychol Psychiatry, 63(7):793-801.

[50]SchoenSA, MillerLJ, Brett-GreenB, et al., 2008. Psychophysiology of children with autism spectrum disorder. Res Autism Spectr Disord, 2(3):417-429.

[51]SchoenSA, MillerLJ, Brett-GreenBA, et al., 2009. Physiological and behavioral differences in sensory processing: a comparison of children with autism spectrum disorder and sensory modulation disorder. Front Integr Neurosci, 3:29.

[52]SchoplerE, ReichlerRJ, DeVellisRF, et al., 1980. Toward objective classification of childhood autism: childhood autism rating scale (CARS). J Autism Dev Disord, 10(1):91-103.

[53]StevensS, GruzelierJ, 1984. Electrodermal activity to auditory stimuli in autistic, retarded, and normal children. J Autism Dev Disord, 14(3):245-260.

[54]StuartN, WhitehouseA, PalermoR, et al., 2023. Eye gaze in autism spectrum disorder: a review of neural evidence for the eye avoidance hypothesis. J Autism Dev Disord, 53:1884-1905.

[55]TakahashiH, NakahachiT, KomatsuS, et al., 2014. Hyperreactivity to weak acoustic stimuli and prolonged acoustic startle latency in children with autism spectrum disorders. Mol Autism, 5:23.

[56]TopDN, LukeSG, StephensonKG, et al., 2019. Psychophysiological arousal and auditory sensitivity in a cross-clinical sample of autistic and non-autistic anxious adults. Front Psychiatry, 9:783.

[57]UljarevićM, BaranekG, VivantiG, et al., 2017. Heterogeneity of sensory features in autism spectrum disorder: challenges and perspectives for future research. Autism Res, 10(5):703-710.

[58]van EngelandH, 1984. The electrodermal orienting response to auditive stimuli in autistic children, normal children, mentally retarded children, and child psychiatric patients. J Autism Dev Disord, 14(3):261-279.

[59]WangCA, BlohmG, HuangJ, et al., 2017. Multisensory integration in orienting behavior: pupil size, microsaccades, and saccades. Biol Psychol, 129:36-44.

[60]WechslerD, 2014. Wechsler Intelligence Scale for Preschool and Primary Children—Fourth CN Edition. Li YQ, Zhu JJ, translators, 2014. King‐May Company, China.

[61]ZhaoSJ, YumNW, BenjaminL, et al., 2019. Rapid ocular responses are modulated by bottom-up-driven auditory salience. J Neurosci, 39(39):7703-7714.