The rubber hand illusion reveals proprioceptive and sensorimotor differences in autism spectrum disorders

Journal of Autism and Developmental Disorders

Volumn 42, Issue 9, 2012, Pages 1870-1883

  Paton, Bryan ^a   Hohwy, Jakob ^a   Enticott, Peter G ^b  

^a MONASH UNIVERSITY   (Australia)

^b NONE   (Australia)

Author keywords

High functioning autism spectrum disorder; Local processing bias; Multimodal sensory integration; Rubber hand illusion

Indexed keywords

ADULT; ARTICLE; AUTISM; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; ILLUSION; MALE; PRIORITY JOURNAL; PROPRIOCEPTION; RUBBER HAND ILLUSION; SENSORIMOTOR FUNCTION; SKIN TEMPERATURE; TACTILE STIMULATION;

ADULT; ASPERGER SYNDROME; AUTISTIC DISORDER; CHILD; FEMALE; HUMANS; ILLUSIONS; MALE; PROPRIOCEPTION; VISUAL PERCEPTION;

EID: 84866739104     PISSN: 01623257     EISSN: 15733432     Source Type: Journal    
DOI: 10.1007/s10803-011-1430-7     Document Type: Article

References (88)

1. Alais, D., & Burr, D. (2004). The ventriloquist effect results from near-optimal bimodal integration. Current Biology, 14, 257-262.
2. Armel, K. C., & Ramachandran, V. S. (2003). Projecting sensations to external objects: Evidence from skin conductance response. Proceedings of the Royal Society of London Series B: Biological Sciences, 270(1523), 1499-1506. doi:10.1098/rspb.2003.2364.
3. Baron-Cohen, S., & Wheelwright, S. (2004). The empathy quotient: An investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34(2), 163-175.
4. Bays, P. M., & Wolpert, D. M. (2007). Computational principles of sensorimotor control that minimize uncertainty and variability. The Journal of Physiology, 578(2), 387-396. doi:10.1113/jphysiol. 2006.120121.
5. Bebko, J. M., Weiss, J. A., Demark, J. L., & Gomez, P. (2006). Discrimination of temporal synchrony in intermodal events by children with autism and children with developmental disabilities without autism. Journal of Child Psychology and Psychiatry, 47(1), 88-98. doi:10.1111/j.1469-7610.2005. 01443.x.
6. Ben-Sasson, A., Hen, L., Fluss, R., Cermak, S., Engel-Yeger, B., & Gal, E. (2009). A meta-analysis of sensory modulation symptoms in individuals with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(1), 1-11. doi: 10.1007/s10803-008-0593-3.
7. Bölte, S., Holtmann, M., Poustka, F., Scheurich, A., & Schmidt, L. (2007). Gestalt perception and local-global processing in highfunctioning autism. Journal of Autism and Developmental Disorders, 37(8), 1493-1504. doi:10.1007/s10803-006-0231-x.
8. Bonnel, A., Mottron, L., Peretz, I., Trudel, M., Gallun, E., & Bonnel, A.-M. (2003). Enhanced pitch sensitivity in individuals with autism: A signal detection analysis. Journal of Cognitive Neuroscience, 15(2), 226-235. doi:10.1162/089892903321208169.
9. Botvinick, M., & Cohen, J. (1998). Rubber hands 'feel' touch that eyes see. Nature, 391(6669), 756.
10. Cascio, C., McGlone, F., Folger, S., Tannan, V., Baranek, G., Pelphrey, K., et al. (2008). Tactile perception in adults with autism: A multidimensional psychophysical study. Journal of Autism and Developmental Disorders, 38(1), 127-137. doi: 10.1007/s10803-007-0370-8.
11. Chong, T. W. H., & Castle, D. J. (2004). Layer upon layer: thermoregulation in schizophrenia. Schizophrenia Research, 69(2-3), 149-157. doi:10.1016/S0920-9964 (03) 00222-6.
12. Dakin, S., & Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497-507. doi:10.1016/j.neuron. 2005.10.018.
13. Desmurget, M., Vindras, P., Gréa, H., Viviani, P., & Grafton, S. T. (2000). Proprioception does not quickly drift during visual occlusion. Experimental Brain Research, 134(3), 363-377.
14. Ehrsson, H. H. (2007). The experimental induction of out-of-body experiences. Science, 317(5841), 1048. doi:10.1126/science. 1142175.
15. Ehrsson, H. H., Spence, C., & Passingham, R. E. (2004). That's my hand! Activity in premotor cortex reflects feeling of ownership of a limb. Science, 305(5685), 875-877.
16. Enticott, P. G., Kennedy, H. A., Bradshaw, J. L., Rinehart, N. J., & Fitzgerald, P. B. (2010). Understanding mirror neurons: Evidence for enhanced corticospinal excitability during the observation of transitive but not intransitive hand gestures. Neuropsychologia, 48(9), 2675-2680. doi:10.1016/j.neuropsychologia.2010.05.014.
17. Enticott, P. G., Kennedy, H. A., Rinehart, N. J., Tonge, B. J. Bradshaw, J. L., Taffe, J. R., et al. (in press). Mirror neuron activity associated with social impairments but not age in autism spectrum disorder. Biological Psychiatry. doi:10.1016/j.biopsych.2011.09.001.
18. Ernst, M., & Banks, M. (2002). Humans integrate visual and haptic information in a statistically optimal fashion. Nature, 415, 429-433.
19. Fiorio, M., Weise, D., Önal-Hartmann, C., Zeller, D., Tinazzi, M., & Classen, J. (2011). Impairment of the rubber hand illusion in focal hand dystonia. Brain, 134(5), 1428-1437. doi:10.1093/brain/awr026.
20. Foss-Feig, J., Kwakye, L., Cascio, C., Burnette, C., Kadivar, H., Stone, W., et al. (2010). An extended multisensory temporal binding window in autism spectrum disorders. Experimental Brain Research, 203(2), 381-389. doi:10.1007/s00221-010-2240-4.
21. Frith, U. (1989). Autism: Explaining the enigma. Oxford: Blackwell.
22. Fuentes, C., Mostofsky, S., & Bastian, A. (2010). No proprioceptive deficits in autism despite movement-related sensory and execution impairments. Journal of Autism and Developmental Disorders, 41(10), 1352-1361.
23. Gallese, V., & Goldman, A. (1998). Mirror neurons and the simulation theory of mind-reading. Trends in Cognitive Sciences, 2, 493-501.
24. Gepner, B., & Mestre, D. R. (2002). Brief report: Postural reactivity to fast visual motion differentiates autistic from children with Asperger syndrome. Journal of Autism and Developmental Disorders, 32(3), 231-238. doi:10.1023/a:1015410015859.
25. Gepner, B., Mestre, D., Masson, G., & de Schonen, S. (1995). Postural effects of motion vision in young autistic children. NeuroReport, 6(8), 1211-1214.
26. Giummarra, M. J., Gibson, S. J., Georgiou-Karistianis, N., & Bradshaw, J. L. (2008). Mechanisms underlying embodiment, disembodiment and loss of embodiment. Neuroscience and Biobehavioral Reviews, 32(1), 143-160. doi:10.1016/j.neubiorev. 2007.07.001.
27. Gross, Y., & Melzack, R. (1978). Body image: Dissociation of real and perceived limbs by pressure-cuff ischemia. Experimental Neurology, 61(3), 680-688. doi:10.1016/0014-4886 (78) 90032-8.
28. Gross, Y., Webb, R., & Melzack, R. (1974). Central and peripheral contributions to localization of body parts: Evidence for a central body schema. Experimental Neurology, 44(3), 346-362. doi: 10.1016/0014-4886 (74) 90201-5.
29. Guterstam, A., Petkova, V. I., & Ehrsson, H. H. (2011). The illusion of owning a third arm. PloS One, 66(2), e17208.
30. Haans, A., Ijsselsteijn, W. A., & de Kort, Y. A. W. (2008). The effect of similarities in skin texture and hand shape on perceived ownership of a fake limb. Body Image, 5(4), 389-394.
31. Happé, F. G. E. (1996). Studying weak central coherence at low levels: Children with autism do not succumb to visual illusions. A research note. Journal of Child Psychology and Psychiatry, 37(7), 873-877. doi:10.1111/j.1469-7610.1996.tb01483.x.
32. Happé, F., & Frith, U. (2006). The weak coherence account: Detailfocused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5-25. doi: 10.1007/s10803-005-0039-0.
33. Haswell, C. C., Izawa, J., Dowell, L. R., Mostofsky, S. H., & Shadmehr, R. (2009). Representation of internal models of action in the autistic brain. Nature Neuroscience, 12(8), 970-972. doi:10.1038/nn. 2356.
34. Hohwy, J., & Paton, B. (2010). Explaining away the body: Experiences of supernaturally caused touch and touch on nonhand objects within the rubber hand illusion. PloS One, 5(2), e9416. http://dx.plos.org/10.1371/journal.pone. 0009416.
35. Hoy, J. A., Hatton, C., & Hare, D. (2004). Weak central coherence: A cross-domain phenomenon specific to autism? Autism, 8(3), 267-281. doi:10.1177/1362361304045218.
36. Iacoboni, M., & Dapretto, M. (2006). The mirror neuron system and the consequences of its dysfunction. Nature Reviews Neuroscience, 7(12), 942-951. doi:10.1038/nrn2024.
37. Iarocci, G., & McDonald, J. (2006). Sensory integration and the perceptual experience of persons with autism. Journal of Autism and Developmental Disorders, 36(1), 77-90. doi:10.1007/s10803-005-0044-3.
38. Ionta, S., Heydrich, L., Lenggenhager, B., Mouthon, M., Fornari, E., Chapuis, D., et al. (2011). Multisensory mechanisms in temporoparietal cortex support self-location and first-person perspective. Neuron, 70(2), 363-374.
39. Jeannerod, M. (1986). Mechanisms of visuomotor coordination: A study in normal and brain-damaged subjects. Neuropsychologia, 24, 41-78.
40. Kaiser, M. D., & Pelphrey, K. A. (2012). Disrupted action perception in autism: Behavioral evidence, neuroendophenotypes, and diagnostic utility. Developmental Cognitive Neuroscience, 2(1), 25-35. doi:10.1016/j.dcn. 2011.05.005.
41. Kammers, M. P. M., de Vignemont, F., Verhagen, L., & Dijkerman, H. C. (2009a). The rubber hand illusion in action. Neuropsychologia, 47(1), 204-211.
42. Kammers, M., Kootker, J., Hogendoorn, H., & Dijkerman, H. (2010). How many motoric body representations can we grasp? Experimental Brain Research, 202(1), 203-212. doi:10.1007/s00221-009-2124-7.
43. Kammers, M. P. M., Longo, M. R., Tsakiris, M., Dijkerman, H. C., & Haggard, P. (2009b). Specificity and coherence of body representations. Perception, 38(12), 1804-1820.
44. Kammers, M. P. M., Rose, K., & Haggard, P. (2011). Feeling numb: Temperature, but not thermal pain, modulates feeling of body ownership. Neuropsychologia, 49(5), 1316-1321. doi: 10.1016/j.neuropsychologia.2011.02.039.
45. Kammers, M. P. M., Verhagen, L., Dijkerman, H. C., Hogendoorn, H., De Vignemont, F., & Schutter, D. J. L. G. (2009c). Is this hand for real? Attenuation of the rubber hand illusion by transcranial magnetic stimulation over the inferior parietal lobule. Journal of Cognitive Neuroscience, 21(7), 1311-1320. doi:10.1162/jocn. 2009.21095.
46. Kording, K., & Wolpert, D. (2004). Bayesian integration in sensorimotor learning. Nature, 427, 244.
47. Kwakye, L. D., Foss-Feig, J. H., Cascio, C. J., Stone, W. L., & Wallace, M. T. (2011). Altered auditory and multisensory temporal processing in autism spectrum disorders. Frontiers in Integrative Neuroscience, 4, 129.
48. Lenggenhager, B., Tadi, T., Metzinger, T., & Blanke, O. (2007). Video ergo sum: Manipulating bodily self-consciousness. Science, 317(5841), 1096.
49. Longo, M. R., Schüür, F., Kammers, M. P. M., Tsakiris, M., & Haggard, P. (2008). What is embodiment? A psychometric approach. Cognition, 107(3), 978-998.
50. Makin, T. R., Holmes, N. P., & Ehrsson, H. H. (2008). On the other hand: Dummy hands and peripersonal space. Behavioural Brain Research, 191(1), 1-10.
51. Mari, M., Castiello, U., Marks, D., Marraffa, C., & Prior, M. (2003). The reach-to-grasp movement in children with autism spectrum disorder. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 393-403.
52. Masterton, B. A., & Biederman, G. B. (1983). Proprioceptive versus visual control in autistic children. Journal of Autism and Developmental Disorders, 13(2), 141-152. doi:10.1007/bf01531815.
53. Moseley, G. L., Gallace, A., & Spence, C. (2012). Bodily illusions in health and disease: Physiological and clinical perspectives and the concept of a cortical 'body matrix'. Neuroscience & Biobehavioral Reviews, 36(1), 34-46. doi:10.1016/j.neubiorev. 2011.03.013.
54. Moseley, G. L., Olthof, N., Venema, A., Don, S., Wijers, M., Gallace, A., et al. (2008). Psychologically induced cooling of a specific body part caused by the illusory ownership of an artificial counterpart. Proceedings of the National Academy of Sciences, 105(35), 13169-13173. doi:10.1073/pnas.0803768105.
55. Mottron, L., Dawson, M., Soulieres, I., Hubert, B., & Burack, J. (2006). Enhanced perceptual functioning in autism: An update, and eight principles of autistic perception. Journal of Autism and Developmental Disorders, 36, 27-43.
56. Mussap, A. J., & Salton, N. (2006). A 'rubber-hand' illusion reveals a relationship between perceptual body image and unhealthy body change. Journal of Health Psychology, 11(4), 627-639. doi: 10.1177/1359105306065022.
57. Nayate, A., Bradshaw, J. L., & Rinehart, N. J. (2005). Autism and Asperger's disorder: Are they movement disorders involving the cerebellum and/or basal ganglia? Brain Research Bulletin, 67(4), 327-334. doi:10.1016/j. brainresbull.2005.07.011.
58. Nazarali, N., Glazebrook, C., & Elliott, D. (2009). Movement planning and reprogramming in individuals with autism. Journal of Autism and Developmental Disorders, 39(10), 1401-1411. doi:10.1007/s10803-009-0756-x.
59. Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cognitive Brain Research, 24(2), 190-198. doi:10.1016/j.cogbrainres.2005.01.014.
60. Peled, A., Pressman, A., Geva, A. B., & Modai, I. (2003). Somatosensory evoked potentials during a rubber-hand illusion in schizophrenia. Schizophrenia Research, 64(2-3), 157-163. doi:10.1016/S0920-9964 (03) 00057-4.
61. Peled, A., Ritsner, M., Hirschmann, S., Geva, A. B., & Modai, I. (2000). Touch feel illusion in schizophrenic patients. Biological Psychiatry, 48(11), 1105-1108.
62. Petkova, V. I., & Ehrsson, H. H. (2008). If I were you: Perceptual illusion of body swapping. PLoS ONE, 3(12), e3832.
63. Recanzone, G. H. (1998). Rapidly induced auditory plasticity: The ventriloquism aftereffect. Proceedings of the National Academy of Sciences, 95(3), 869-875.
64. Rinehart, N., Bradshaw, J., Brereton, A., & Tonge, B. (2001). Movement preparation in high-functioning autism and Asperger disorder: A serial choice reaction time task involving motor reprogramming. Journal of Autism and Developmental Disorders, 31(1), 79-88. doi:10.1023/a:1005617831035.
65. Rinehart, N. J., Tonge, B. J., Bradshaw, J. L., Iansek, R., Enticott, P. G., & Johnson, K. A. (2006). Movement-related potentials in high-functioning autism and Asperger's disorder. Developmental Medicine and Child Neurology, 48(4), 272-277. doi:10.1017/s0012162206000594.
66. Rippon, G., Brock, J., Brown, C., & Boucher, J. (2007). Disordered connectivity in the autistic brain: Challenges for the 'new psychophysiology'. International Journal of Psychophysiology, 63(2), 164-172. doi:10.1016/j. ijpsycho.2006.03.012.
67. Rogers, S. J., Cook, I., & Meryl, A. (2005). Imitation and play in autism. In F. R. Volkmar, R. Paul, A. Klin, & D. Cohen (Eds.), Handbook of autism and pervasive developmental disorders (3rd ed., pp. 382-405). Hoboken, NJ: Wiley.
68. Rogers, S. J., & Ozonoff, S. (2005). Annotation: What do we know about sensory dysfunction in autism? A critical review of the empirical evidence. Journal of Child Psychology and Psychiatry, 46(12), 1255-1268. doi:10.1111/j.1469-7610.2005.01431.x.
69. Rohde, M., Di Luca, M., & Ernst, M. O. (2011). The rubber hand illusion: Feeling of ownership and proprioceptive drift do not go hand in hand. PloS One, 6(6), e21659.
70. Ropar, D., & Mitchell, P. (1999). Are individuals with autism and Asperger's syndrome susceptible to visual illusions? Journal of Child Psychology and Psychiatry, 40(8), 1283-1293. doi: 10.1111/1469-7610.00544.
71. Ropar, D., & Mitchell, P. (2001). Susceptibility to illusions and performance on visuospatial tasks in individuals with autism. Journal of Child Psychology and Psychiatry, 42(4), 539-549. doi:10.1111/1469-7610.00748.
72. Ropar, D., & Mitchell, P. (2002). Shape constancy in autism: The role of prior knowledge and perspective cues. Journal of Child Psychology and Psychiatry, 43(5), 647-653. doi:10.1111/1469-7610.00053.
73. Rossetti, Y., Desmurget, M., & Prablanc, C. (1995). Vectorial coding of movement: Vision, proprioception, or both? Journal of Neurophysiology, 74(1), 457-463.
74. Schwabe, L., & Blanke, O. (2008). The vestibular component in outof-body experiences: a computational approach. Frontiers in Human Neuroscience, 2(Article 17), 1-10.
75. Simmons, D. R., Robertson, A. E., McKay, L. S., Toal, E., McAleer, P., & Pollick, F. E. (2009). Vision in autism spectrum disorders. Vision Research, 49(22), 2705-2739. doi:10.1016/j.visres.2009. 08.005.
76. Smith, E. G., & Bennetto, L. (2007). Audiovisual speech integration and lipreading in autism. Journal of Child Psychology and Psychiatry, 48(8), 813-821. doi:10.1111/j.1469-7610.2007.01766.x.
77. Sober, S. J., & Sabes, P. N. (2003). Multisensory integration during motor planning. The Journal of Neuroscience, 23(18), 6982-6992.
78. Sober, S. J., & Sabes, P. N. (2005). Flexible strategies for sensory integration during motor planning. Nature Neuroscience, 8, 490-497.
79. Théoret, H., Halligan, E., Kobayashi, M., Fregni, F., Tager-Flusberg, H., & Pascual-Leone, A. (2005). Impaired motor facilitation during action observation in individuals with autism spectrum disorder. Current Biology, 15(3), R84-R85.
80. Tsakiris, M. (2010). My body in the brain: A neurocognitive model of body-ownership. Neuropsychologia, 48(3), 703-712. doi: 10.1016/j. neuropsychologia.2009.09.034.
81. Tsakiris, M., Carpenter, L., James, D., & Fotopoulou, A. (2010). Hands only illusion: multisensory integration elicits sense of ownership for body parts but not for non-corporeal objects. Experimental Brain Research, 204(3), 343-352. doi: 10.1007/s00221-009-2039-3.
82. Tsakiris, M., & Haggard, P. (2005). The rubber hand illusion revisited: Visuotactile integration and self-attribution. Journal of Experimental Psychology: Human Perception and Performance, 31(1), 80-91.
83. van Beers, R. J., Sittig, A. C., & van der Gon, J. J. D. (1999). Integration of proprioceptive and visual position-information: An experimentally supported model. Journal of Neurophysiology, 81(3), 1355-1364.
84. van Beers, R. J., Wolpert, D. M., & Haggard, P. (2002). When feeling is more important than seeing in sensorimotor adaptation. Current Biology, 12(10), 834-837. doi:10.1016/S0960-9822 (02) 00836-9.
85. Walter, E., Dassonville, P., & Bochsler, T. (2009). A specific autistic trait that modulates visuospatial illusion susceptibility. Journal of Autism and Developmental Disorders, 39(2), 339-349. doi: 10.1007/s10803-008- 0630-2.
86. Wann, J. P., & Ibrahim, S. F. (1992). Does limb proprioception drift? Experimental Brain Research, 91(1), 162-166. doi:10.1007/bf00230024.
87. Williams, J. H. G., Whiten, A., Suddendorf, T., & Perrett, D. I. (2001). Imitation, mirror neurons and autism. Neuroscience and Biobehavioral Reviews, 25(4), 287-295. doi:10.1016/S0149-7634 (01) 00014-8.
88. Zopf, R., Truong, S., Finkbeiner, M., Friedman, J., & Williams, M. A. (2011). Viewing and feeling touch modulates hand position for reaching. Neuropsychologia, 49(5), 1287-1293. doi:10.1016/j.neuropsychologia.2011.02.012.