Abstract
While research regarding emotion recognition in ASD has focused primarily on social cues, musical stimuli also elicit strong emotional responses. This study extends and expands the few previous studies of response to music in ASD, measuring both psychophysiological and behavioral responses in younger children (ages 8–11) as well as older adolescents (ages 16–18). Compared to controls, the ASD group demonstrated reduced skin conductance response to music-evoked emotion. Younger groups, regardless of diagnosis, showed greater physiological reactivity to scary stimuli than to other emotions. There was a significant interaction of age group and diagnostic group in identifying scary music stimuli, possibly evidencing disrupted developmental trajectories in ASD for integrating physiological and cognitive cues that may underlie symptoms of anxiety.
Similar content being viewed by others
References
Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience, 14(8), 1264–1274. doi:10.1162/089892902760807258.
Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31(3), 137–145. doi:10.1016/j.tins.2007.12.005.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.
Aubé, W., Angulo-Perkins, A., Peretz, I., Concha, L., & Armony, J. L. (2015). Fear across the senses: Brain responses to music, vocalizations and facial expressions. Social Cognitive and Affective Neuroscience, 10(3), 399–407. doi:10.1093/scan/nsu067.
Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001). The autism-spectrum quotient (AQ): Evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31(1), 5–17.
Berkowitz, R. L., Coplan, J. D., Reddy, D. P., & Gorman, J. M. (2007). The human dimension: How the prefrontal cortex modulates the subcortical fear response. Reviews in the Neurosciences, 18(3–4), 191–207.
Bhatara, A. K., Quintin, E.-M., Heaton, P., Fombonne, E., & Levitin, D. J. (2009). The effect of music on social attribution in adolescents with autism spectrum disorders. Child Neuropsychology, 15(4), 375–396. doi:10.1080/09297040802603653.
Bradley, M. M., & Lang, P. J. (1994). Measuring emotion: The self-assessment manikin and the semantic differential. Journal of Behavior Therapy and Experimental Psychiatry, 25(1), 49–59. doi:10.1016/0005-7916(94)90063-9.
Chamberlain, P. D., Rodgers, J., Crowley, M. J., White, S. E., Freeston, M. H., & South, M. (2013). A potentiated startle study of uncertainty and contextual anxiety in adolescents diagnosed with autism spectrum disorder. Molecular Autism, 4(1), 31. doi:10.1186/2040-2392-4-31.
Conner, C. M., Maddox, B. B., & White, S. W. (2013). Parents’ state and trait anxiety: Relationships with anxiety severity and treatment response in adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 43(8), 1811–1818. doi:10.1007/s10803-012-1728-0.
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., et al. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433. doi:10.1023/A:1025014929212.
Daly, E. M., Deeley, Q., Ecker, C., Craig, M., Hallahan, B., Murphy, C., & Murphy, D. G. M. (2012). Serotonin and the neural processing of facial emotions in adults with autism: An fMRI study using acute tryptophan depletion. JAMA Psychiatry, 69(10), 1003–1013.
Demenescu, L. R., Kortekaas, R., den Boer, J. A., & Aleman, A. (2010). Impaired attribution of emotion to facial expressions in anxiety and major depression. PLoS One. doi:10.1371/journal.pone.0015058.
Deschamps, P. K. H., Coppes, L., Kenemans, J. L., Schutter, D. J. L. G., & Matthys, W. (2013). Electromyographic responses to emotional facial expressions in 6–7 year olds with autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(2), 354–362. doi:10.1007/s10803-013-1890-z.
Easter, J., McClure, E. B., Monk, C. S., Dhanani, M., Hodgdon, H., Leibenluft, E., et al. (2005). Emotion recognition deficits in pediatric anxiety disorders: Implications for amygdala research. Journal of Child and Adolescent Psychopharmacology, 15(4), 563–570. doi:10.1089/cap.2005.15.563.
Ecker, C., Suckling, J., Deoni, S. C., Lombardo, M. V., Bullmore, E. T., Baron-Cohen, S., et al. (2012). Brain anatomy and its relationship to behavior in adults with autism spectrum disorder: A multicenter magnetic resonance imaging study. Archives of General Psychiatry, 69(2), 195–209. doi:10.1001/archgenpsychiatry.2011.1251.
Ewing, L., Pellicano, E., & Rhodes, G. (2013). Using effort to measure reward value of faces in children with autism. PLoS One. doi:10.1371/journal.pone.0079493.
Gosselin, N., Peretz, I., Johnsen, E., & Adolphs, R. (2007). Amygdala damage impairs emotion recognition from music. Neuropsychologia, 45(2), 236–244. doi:10.1016/j.neuropsychologia.2006.07.012.
Gotham, K., Bishop, S. L., Hus, V., Huerta, M., Lund, S., Buja, A., et al. (2013). Exploring the relationship between anxiety and insistence on sameness in autism spectrum disorders. Autism Research, 6(1), 33–41. doi:10.1002/aur.1263.
Greimel, E., Nehrkorn, B., Schulte-Rüther, M., Fink, G. R., Nickl-Jockschat, T., Herpertz-Dahlmann, B., et al. (2013). Changes in grey matter development in autism spectrum disorder. Brain Structure and Function, 218(4), 929–942. doi:10.1007/s00429-012-0439-9.
Greimel, E., Schulte-Rüther, M., Kamp-Becker, I., Remschmidt, H., Herpertz-Dahlmann, B., & Konrad, K. (2014). Impairment in face processing in autism spectrum disorder: A developmental perspective. Journal of Neural Transmission, 121(9), 1171–1181. doi:10.1007/s00702-014-1206-2.
Hattingh, C. J., Ipser, J., Tromp, S. A., Syal, S., Lochner, C., Brooks, S. J., & Stein, D. J. (2013). Functional magnetic resonance imaging during emotion recognition in social anxiety disorder: An activation likelihood meta-analysis. Frontiers in Human Neuroscience, 6, 347. doi:10.3389/fnhum.2012.00347.
Jou, R. J., Jackowski, A. P., Papademetris, X., Rajeevan, N., Staib, L. H., & Volkmar, F. R. (2011). Diffusion tensor imaging in autism spectrum disorders: Preliminary evidence of abnormal neural connectivity. Australian and New Zealand Journal of Psychiatry, 45(2), 153–162. doi:10.3109/00048674.2010.534069.
Juslin, P. N. (2001). Communicating emotion in music performance: A review and a theoretical framework. In P. N. Juslin & J. A. Sloboda (Eds.), Music and emotion: Theory and research (pp. 309–337). New York, NY, US: Oxford University Press.
Kennedy, D. P., & Adolphs, R. (2012). Perception of emotions from facial expressions in high-functioning adults with autism. Neuropsychologia, 50(14), 3313–3319. doi:10.1016/j.neuropsychologia.2012.09.038.
Khalfa, S., Roy, M., Rainville, P., Dalla Bella, S., & Peretz, I. (2008). Role of tempo entrainment in psychophysiological differentiation of happy and sad music? International Journal of Psychophysiology, 68(1), 17–26. doi:10.1016/j.ijpsycho.2007.12.001.
Koelsch, S. (2014). Brain correlates of music-evoked emotions. Nature Reviews Neuroscience, 15(3), 170–180. doi:10.1038/nrn3666.
Kushki, A., Drumm, E., Pla Mobarak, M., Tanel, N., Dupuis, A., Chau, T., & Anagnostou, E. (2013). Investigating the autonomic nervous system response to anxiety in children with autism spectrum disorders. PLoS One. doi:10.1371/journal.pone.0059730.
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1998). Emotion and motivation: Measuring affective perception. Journal of Clinical Neurophysiology, 15(5), 397–408.
Larsen, J. T., Berntson, G. G., Poehlmann, K. M., Ito, T. A., & Cacioppo, J. T. (2008). The psychophysiology of emotion. Handbook of emotions (3rd ed., pp. 180–195). New York, NY: Guilford Press.
Lee, T. C., Dupuis, A., Jones, E., Guberman, C., Herbert, M., & Manassis, K. (2013). Effects of age and subtype on emotional recognition in children with anxiety disorders: Implications for cognitive-behavioural therapy. Canadian Journal of Psychiatry, 58(5), 283–290.
Lord, C., Risi, S., Lambrecht, L., Cook, E. H, Jr, Leventhal, B. L., DiLavore, P. C., et al. (2000). The Autism Diagnostic Observation Schedule—Generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223. doi:10.1023/A:1005592401947.
Louwerse, A., Tulen, J. H. M., van der Geest, J. N., van der Ende, J., Verhulst, F. C., & Greaves-Lord, K. (2014). Autonomic responses to social and nonsocial pictures in adolescents with autism spectrum disorder. Autism Research, 7(1), 17–27. doi:10.1002/aur.1327.
Luke, L., Clare, I. C. H., Ring, H., Redley, M., & Watson, P. (2012). Decision-making difficulties experienced by adults with autism spectrum conditions. Autism, 16(6), 612–621. doi:10.1177/1362361311415876.
Lundqvist, L.-O., Carlsson, F., Hilmersson, P., & Juslin, P. N. (2009). Emotional responses to music: Experience, expression, and physiology. Psychology of Music, 37(1), 61–90. doi:10.1177/0305735607086048.
McIntosh, D. N., Miller, L. J., & Shyu, V. (1999). Development and validation of the short sensory profile. In W. Dunn (Ed.), Sensory profile manual (pp. 59–73). San Antonio, TX: Psychological Corporation.
Monk, C. S., Peltier, S. J., Wiggins, J. L., Weng, S.-J., Carrasco, M., Risi, S., & Lord, C. (2009). Abnormalities of intrinsic functional connectivity in autism spectrum disorders. NeuroImage, 47(2), 764–772. doi:10.1016/j.neuroimage.2009.04.069.
Nauta, M. H., Scholing, A., Rapee, R. M., Abbott, M., Spence, S. H., & Waters, A. (2004). A parent-report measure of children’s anxiety: Psychometric properties and comparison with child-report in a clinic and normal sample. Behaviour Research and Therapy, 42(7), 813–839. doi:10.1016/S0005-7967(03)00200-6.
Nickl-Jockschat, T., Rottschy, C., Thommes, J., Schneider, F., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2014). Neural networks related to dysfunctional face processing in autism spectrum disorder. Brain Structure and Function, 220(4), 2355–2371. doi:10.1007/s00429-014-0791-z.
Ozsivadjian, A., & Knott, F. (2011). Anxiety problems in young people with autism spectrum disorder: A case series. Clinical Child Psychology and Psychiatry, 16(2), 203–214. doi:10.1177/1359104511404749.
Pessoa, L., & Adolphs, R. (2010). Emotion processing and the amygdala: From a “low road” to “many roads” of evaluating biological significance. Nature Reviews Neuroscience, 11(11), 773–783. doi:10.1038/nrn2920.
Quintin, E.-M., Bhatara, A., Poissant, H., Fombonne, E., & Levitin, D. J. (2011). Emotion perception in music in high-functioning adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 41(9), 1240–1255. doi:10.1007/s10803-010-1146-0.
Riby, D. M., Hanley, M., Kirk, H., Clark, F., Little, K., Fleck, R., et al. (2014). The interplay between anxiety and social functioning in Williams syndrome. Journal of Autism and Developmental Disorders, 44(5), 1220–1229. doi:10.1007/s10803-013-1984-7.
Rodgers, J., Glod, M., Connolly, B., & McConachie, H. (2012). The relationship between anxiety and repetitive behaviours in autism spectrum disorder. Journal of Autism and Developmental Disorders, 42(11), 2404–2409. doi:10.1007/s10803-012-1531-y.
Roy, M., Mailhot, J.-P., Gosselin, N., Paquette, S., & Peretz, I. (2009). Modulation of the startle reflex by pleasant and unpleasant music. International Journal of Psychophysiology, 71(1), 37–42. doi:10.1016/j.ijpsycho.2008.07.010.
Schultz, R. T. (2005). Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23(2–3), 125–141. doi:10.1016/j.ijdevneu.2004.12.012.
Schumann, C. M., Hamstra, J., Goodlin-Jones, B. L., Lotspeich, L. J., Kwon, H., Buonocore, M. H., et al. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. The Journal of Neuroscience, 24(28), 6392–6401. doi:10.1523/JNEUROSCI.1297-04.2004.
Shafritz, K. M., Bregman, J. D., Ikuta, T., & Szeszko, P. R. (2015). Neural systems mediating decision-making and response inhibition for social and nonsocial stimuli in autism. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 60, 112–120. doi:10.1016/j.pnpbp.2015.03.001.
Shin, L. M., & Liberzon, I. (2009). The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology, 35(1), 169–191. doi:10.1038/npp.2009.83.
Song, Y., & Hakoda, Y. (2012). The interference of local over global information processing in children with attention deficit hyperactivity disorder of the inattentive type. Brain and Development, 34(4), 308–317. doi:10.1016/j.braindev.2011.07.010.
South, M., Chamberlain, P. D., Wigham, S., Newton, T., Le Couteur, A., McConachie, H., et al. (2014). Enhanced decision making and risk avoidance in high-functioning autism spectrum disorder. Neuropsychology, 28(2), 222–228. doi:10.1037/neu0000016.
South, M., Newton, T., & Chamberlain, P. D. (2012). Delayed reversal learning and association with repetitive behavior in autism spectrum disorders. Autism Research, 5(6), 398–406. doi:10.1002/aur.1255.
South, M., Ozonoff, S., Suchy, Y., Kesner, R. P., McMahon, W. M., & Lainhart, J. E. (2008). Intact emotion facilitation for nonsocial stimuli in autism: Is amygdala impairment in autism specific for social information? Journal of the International Neuropsychological Society, 14(01), 42–54. doi:10.1017/S1355617708080107.
Spence, S. H. (1998). A measure of anxiety symptoms among children. Behaviour Research and Therapy, 36(5), 545–566.
Tanaka, J. W., Wolf, J. M., Klaiman, C., Koenig, K., Cockburn, J., Herlihy, L., et al. (2012). The perception and identification of facial emotions in individuals with autism spectrum disorders using the Let’s Face It! Emotion Skills Battery. Journal of Child Psychology and Psychiatry, 53(12), 1259–1267. doi:10.1111/j.1469-7610.2012.02571.x.
Uljarevic, M., & Hamilton, A. (2013). Recognition of emotions in autism: A formal meta-analysis. Journal of Autism and Developmental Disorders, 43(7), 1517–1526. doi:10.1007/s10803-012-1695-5.
van Steensel, F. J. A., Bögels, S. M., & Perrin, S. (2011). Anxiety disorders in children and adolescents with autistic spectrum disorders: A meta-analysis. Clinical Child and Family Psychology Review, 14(3), 302–317. doi:10.1007/s10567-011-0097-0.
Vasa, R. A., Kalb, L., Mazurek, M., Kanne, S., Freedman, B., Keefer, A., et al. (2013). Age-related differences in the prevalence and correlates of anxiety in youth with autism spectrum disorders. Research in Autism Spectrum Disorders, 7(11), 1358–1369. doi:10.1016/j.rasd.2013.07.005.
von dem Hagen, E. A. H., Stoyanova, R. S., Baron-Cohen, S., & Calder, A. J. (2013). Reduced functional connectivity within and between “social” resting state networks in autism spectrum conditions. Social Cognitive and Affective Neuroscience, 8(6), 694–701. doi:10.1093/scan/nss053.
White, S. W., Mazefsky, C. A., Dichter, G. S., Chiu, P. H., Richey, J. A., & Ollendick, T. H. (2014). Social-cognitive, physiological, and neural mechanisms underlying emotion regulation impairments: Understanding anxiety in autism spectrum disorder. International Journal of Developmental Neuroscience, 39, 22–36. doi:10.1016/j.ijdevneu.2014.05.012.
White, S. W., Oswald, D., Ollendick, T., & Scahill, L. (2009). Anxiety in children and adolescents with autism spectrum disorders. Clinical Psychology Review, 29(3), 216–229. doi:10.1016/j.cpr.2009.01.003.
Williams, D., & Happé, F. (2010). Recognising “social” and “non-social” emotions in self and others: A study of autism. Autism, 14(4), 285–304. doi:10.1177/1362361309344849.
Wong, N., Beidel, D. C., Sarver, D. E., & Sims, V. (2012). Facial emotion recognition in children with high functioning autism and children with social phobia. Child Psychiatry and Human Development, 43(5), 775–794. doi:10.1007/s10578-012-0296-z.
Worsham, W., Gray, W. E., Larson, M. J., & South, M. (2014). Conflict adaptation and congruency sequence effects to social–emotional stimuli in individuals with autism spectrum disorders. Autism. doi:10.1177/1362361314553280. (Advance online publication).
Acknowledgments
We thank our study participants and their families for their willingness to participate in this research. Special thanks to Porter Charles for design of the self-assessment manikins. This research was supported by a College of Family, Home and Social Sciences Research Award from Brigham Young University.
Author Contributions
KGS conceived of the study, participated in the design and coordination (including data acquisition), performed the statistical analyses, and drafted the manuscript. EMQ helped with study conception and design, data interpretation, and drafting of manuscript. MS also helped with study conception and design, data interpretation, and drafting of manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Appendix
Appendix
See Table 1.
Rights and permissions
About this article
Cite this article
Stephenson, K.G., Quintin, E.M. & South, M. Age-Related Differences in Response to Music-Evoked Emotion Among Children and Adolescents with Autism Spectrum Disorders. J Autism Dev Disord 46, 1142–1151 (2016). https://doi.org/10.1007/s10803-015-2624-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-015-2624-1