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Journal of Autism and Developmental Disorders

Gepubliceerd in:

01-09-2012 | Original paper

The Rubber Hand Illusion Reveals Proprioceptive and Sensorimotor Differences in Autism Spectrum Disorders

Auteurs: Bryan Paton, Jakob Hohwy, Peter G. Enticott

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 9/2012

Abstract

Autism spectrum disorder (ASD) is characterised by differences in unimodal and multimodal sensory and proprioceptive processing, with complex biases towards local over global processing. Many of these elements are implicated in versions of the rubber hand illusion (RHI), which were therefore studied in high-functioning individuals with ASD and a typically developing control group. Both groups experienced the illusion. A number of differences were found, related to proprioception and sensorimotor processes. The ASD group showed reduced sensitivity to visuotactile-proprioceptive discrepancy but more accurate proprioception. This group also differed on acceleration in subsequent reach trials. Results are discussed in terms of weak top-down integration and precision-accuracy trade-offs. The RHI appears to be a useful tool for investigating multisensory processing in ASD.

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Alais, D., & Burr, D. (2004). The ventriloquist effect results from near-optimal bimodal integration. Current Biology, 14, 257–262.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Bölte, S., Holtmann, M., Poustka, F., Scheurich, A., & Schmidt, L. (2007). Gestalt perception and local-global processing in high-functioning autism. Journal of Autism and Developmental Disorders, 37(8), 1493–1504. doi:10.1007/s10803-006-0231-x.PubMedCrossRef

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.PubMedCrossRef

Botvinick, M., & Cohen, J. (1998). Rubber hands ‘feel’ touch that eyes see. Nature, 391(6669), 756.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Dakin, S., & Frith, U. (2005). Vagaries of visual perception in autism. Neuron, 48(3), 497–507. doi:10.1016/j.neuron.2005.10.018.PubMedCrossRef

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.CrossRef

Ehrsson, H. H. (2007). The experimental induction of out-of-body experiences. Science, 317(5841), 1048. doi:10.1126/science.1142175.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.

Ernst, M., & Banks, M. (2002). Humans integrate visual and haptic information in a statistically optimal fashion. Nature, 415, 429–433.

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.PubMedCrossRef

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.CrossRef

Frith, U. (1989). Autism: Explaining the enigma. Oxford: Blackwell.

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.

Gallese, V., & Goldman, A. (1998). Mirror neurons and the simulation theory of mind-reading. Trends in Cognitive Sciences, 2, 493–501.PubMedCrossRef

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.PubMedCrossRef

Gepner, B., Mestre, D., Masson, G., & de Schonen, S. (1995). Postural effects of motion vision in young autistic children. NeuroReport, 6(8), 1211–1214.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Guterstam, A., Petkova, V. I., & Ehrsson, H. H. (2011). The illusion of owning a third arm. PloS One, 6(2), e17208.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Happé, F., & Frith, U. (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5–25. doi:10.1007/s10803-005-0039-0.PubMedCrossRef

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.

Hohwy, J., & Paton, B. (2010). Explaining away the body: Experiences of supernaturally caused touch and touch on non-hand objects within the rubber hand illusion. PloS One, 5(2), e9416. http://dx.plos.org/10.1371/journal.pone.0009416.

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Ionta, S., Heydrich, L., Lenggenhager, B., Mouthon, M., Fornari, E., Chapuis, D., et al. (2011). Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron, 70(2), 363–374.PubMedCrossRef

Jeannerod, M. (1986). Mechanisms of visuomotor coordination: A study in normal and brain-damaged subjects. Neuropsychologia, 24, 41–78.PubMedCrossRef

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.

Kammers, M. P. M., de Vignemont, F., Verhagen, L., & Dijkerman, H. C. (2009a). The rubber hand illusion in action. Neuropsychologia, 47(1), 204–211.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Kording, K., & Wolpert, D. (2004). Bayesian integration in sensorimotor learning. Nature, 427, 244.PubMedCrossRef

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.PubMedCrossRef

Lenggenhager, B., Tadi, T., Metzinger, T., & Blanke, O. (2007). Video ergo sum: Manipulating bodily self-consciousness. Science, 317(5841), 1096.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.

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.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Peled, A., Ritsner, M., Hirschmann, S., Geva, A. B., & Modai, I. (2000). Touch feel illusion in schizophrenic patients. Biological Psychiatry, 48(11), 1105–1108.PubMedCrossRef

Petkova, V. I., & Ehrsson, H. H. (2008). If I were you: Perceptual illusion of body swapping. PLoS ONE, 3(12), e3832.PubMedCrossRef

Recanzone, G. H. (1998). Rapidly induced auditory plasticity: The ventriloquism aftereffect. Proceedings of the National Academy of Sciences, 95(3), 869–875.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Rossetti, Y., Desmurget, M., & Prablanc, C. (1995). Vectorial coding of movement: Vision, proprioception, or both? Journal of Neurophysiology, 74(1), 457–463.PubMed

Schwabe, L., & Blanke, O. (2008). The vestibular component in out-of-body experiences: a computational approach. Frontiers in Human Neuroscience, 2(Article 17), 1–10.

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.PubMedCrossRef

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.PubMedCrossRef

Sober, S. J., & Sabes, P. N. (2003). Multisensory integration during motor planning. The Journal of Neuroscience, 23(18), 6982–6992.PubMed

Sober, S. J., & Sabes, P. N. (2005). Flexible strategies for sensory integration during motor planning. Nature Neuroscience, 8, 490–497.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

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.CrossRef

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.PubMedCrossRef

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.PubMed

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.PubMedCrossRef

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.PubMedCrossRef

Wann, J. P., & Ibrahim, S. F. (1992). Does limb proprioception drift? Experimental Brain Research, 91(1), 162–166. doi:10.1007/bf00230024.CrossRef

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.PubMedCrossRef

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.PubMedCrossRef

Titel: The Rubber Hand Illusion Reveals Proprioceptive and Sensorimotor Differences in Autism Spectrum Disorders
Auteurs: Bryan Paton
Jakob Hohwy
Peter G. Enticott
Publicatiedatum: 01-09-2012
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 9/2012
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-011-1430-7

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