RESEARCH ARTICLE
The Action Observation System when Observing Hand Actions in Autism and Typical Development
Jennifer J. Pokorny,
Naomi V. Hatt,
Costanza Colombi,
Giacomo Vivanti,
Sally J. Rogers,
Susan M. Rivera,
Jennifer J. Pokorny
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Psychiatry and Behavioral Sciences, University of California Davis, Sacramento, California, 95817
Center for Mind and Brain, University of California Davis, Davis, California, 95618
Search for more papers by this authorNaomi V. Hatt
Department of Psychology, University of California Davis, Davis, California, 95616
Center for Mind and Brain, University of California Davis, Davis, California, 95618
Search for more papers by this authorCostanza Colombi
University of Michigan, Ann Arbor, Michigan, 48109
Search for more papers by this authorGiacomo Vivanti
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Psychiatry and Behavioral Sciences, University of California Davis, Sacramento, California, 95817
Search for more papers by this authorSally J. Rogers
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Psychiatry and Behavioral Sciences, University of California Davis, Sacramento, California, 95817
Search for more papers by this authorCorresponding Author
Susan M. Rivera
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Department of Psychology, University of California Davis, Davis, California, 95616
Center for Mind and Brain, University of California Davis, Davis, California, 95618
Address for Correspondence and reprints: Susan M. Rivera, The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, CA 95817. E-mail: [email protected]Search for more papers by this authorJennifer J. Pokorny,
Naomi V. Hatt,
Costanza Colombi,
Giacomo Vivanti,
Sally J. Rogers,
Susan M. Rivera,
Jennifer J. Pokorny
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Psychiatry and Behavioral Sciences, University of California Davis, Sacramento, California, 95817
Center for Mind and Brain, University of California Davis, Davis, California, 95618
Search for more papers by this authorNaomi V. Hatt
Department of Psychology, University of California Davis, Davis, California, 95616
Center for Mind and Brain, University of California Davis, Davis, California, 95618
Search for more papers by this authorCostanza Colombi
University of Michigan, Ann Arbor, Michigan, 48109
Search for more papers by this authorGiacomo Vivanti
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Psychiatry and Behavioral Sciences, University of California Davis, Sacramento, California, 95817
Search for more papers by this authorSally J. Rogers
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Psychiatry and Behavioral Sciences, University of California Davis, Sacramento, California, 95817
Search for more papers by this authorCorresponding Author
Susan M. Rivera
The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, California, 95817
Department of Psychology, University of California Davis, Davis, California, 95616
Center for Mind and Brain, University of California Davis, Davis, California, 95618
Address for Correspondence and reprints: Susan M. Rivera, The MIND (Medical Investigation of Neurodevelopmental Disorders) Institute, University of California Davis Medical Center, Sacramento, CA 95817. E-mail: [email protected]Search for more papers by this authorAbstract
Social impairments in individuals with autism spectrum disorders (ASD) may be in part due to difficulty perceiving and recognizing the actions of others. Evidence from imitation studies, which involves both observation and execution of an action, suggests differences, in individuals with ASD, between the ability to imitate goal-directed actions involving objects (transitive actions) and the ability to imitate actions that do not involve objects (intransitive actions). In the present study, we examined whether there were differences in how ASD adolescents encoded transitive and intransitive actions compared to typically developing (TD) adolescents, by having participants view videos of a hand reaching across a screen toward an object or to where an object would be while functional magnetic resonance images were collected. Analyses focused on areas within the action observation network (AON), which is activated during the observation of actions performed by others. We hypothesized that the AON would differentiate transitive from intransitive actions only in the ASD group. However, results revealed that object presence modulated activity in the right inferior frontal gyrus and supramarginal gyrus of the TD group, a differentiation that was not seen in the ASD group. Furthermore, there were no significant group differences between the TD and ASD groups in any of the conditions. This suggests that there is not a global deficit of the AON in individuals with ASD while observing transitive and intransitive actions. Autism Res 2015, 8: 284–296. © 2015 International Society for Autism Research, Wiley Periodicals, Inc.
References
- Agnew, Z.K., Wise, R.J., & Leech, R. (2012). Dissociating object directed and non-object directed action in the human mirror system; implications for theories of motor simulation. PloS One, 7(4), e32517.
- American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders ( 5th ed.) Arlington, VA: American Psychiatric Publishing.
10.1176/appi.books.9780890425596 Google Scholar
- Bastiaansen, J.A., Thioux, M., Nanetti, L., van der Gaag, C., Ketelaars, C., Minderaa, R., et al. (2011). Age-Related increase in inferior frontal gyrus activity and social functioning in autism spectrum disorder. Biological Psychiatry, 69(9), 832–838.
- Bonda, E., Petrides, M., Ostry, D., & Evans, A. (1996). Specific involvement of human parietal systems and the amygdala in the perception of biological motion. The Journal of Neuroscience, 16(11), 3737–3744.
- Bonini, L., Rozzi, S., Serventi, F.U., Simone, L., Ferrari, P.F., & Fogassi, L. (2010). Ventral premotor and inferior parietal cortices make distinct contribution to action organization and intention understanding. Cerebral Cortex, 20(6), 1372–1385.
- Brett, M., Anton, J., Valabregue, R., & Poline, J. (2002). Region of interest analysis using an SPM toolbox [abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, June 2–6, 2002, Sendai, Japan. NeuroImage, 16(2), Abstract 497.
- Buccino, G., Binkofski, F., Fink, G.R., Fadiga, L., Fogassi, L., Gallese, V., et. al. (2001). Action observation activates premotor and parietal areas in a somatotopic manner: An fMRI study. The European Journal of Neuroscience, 13(2), 400–404.
- Buccino, G., Vogt, S., Ritzl, A., Fink, G.R., Zilles, K., Freund, H.-J., et. al. (2004). Neural circuits underlying imitation learning of hand actions: An event-related fMRI study. Neuron, 42(2), 323–334.
- Caspers, S., Zilles, K., Laird, A.R., & Eickhoff, S.B. (2010). ALE meta-analysis of action observation and imitation in the human brain. NeuroImage, 50(3), 1148–1167.
- Cochin, S., Barthelemy, C., Roux, S., & Martineau, J. (1999). Observation and execution of movement: Similarities demonstrated by quantified electroencephalography. The European Journal of Neuroscience, 11(5), 1839–1842.
- Colombi, C., Vivanti, G., & Rogers, S. (2011). The neuropsychology of imitation deficit in autism. In D. Fein (Ed.), The neuropsychology of autism (pp. 243–266). New York, NY: Oxford University Press.
- Corina, D., Chiu, Y.S., Knapp, H., Greenwald, R., San Jose-Robertson, L., & Braun, A. (2007). Neural correlates of human action observation in hearing and deaf subjects. Brain Research, 1152, 111–129.
- Dapretto, M., Davies, M.S., Pfeifer, J.H., Scott, A.A., Sigman, M., Bookheimer, S.Y., et. al. (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9(1), 28–30.
- Decety, J., & Grèzes, J. (1999). Neural mechanisms subserving the perception of human actions. Trends in Cognitive Sciences, 3(5), 172–178.
- Decety, J., Grezes, J., Costes, N., Perani, D., Jeannerod, M., Procyk, E., et al. (1997). Brain activity during observation of actions. Influence of action content and subject's strategy. Brain, 120(10), 1763.
- di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91, 176–180.
- Dinstein, I., Thomas, C., Humphreys, K., Minshew, N., Behrmann, M., & Heeger, D.J. (2010). Normal movement selectivity in autism. Neuron, 66(3), 461–469.
- Edwards, L.A. (2014). A meta-analysis of imitation abilities in individuals with autism specturm disorders. Autism Research, 7(3), 363–380.
- Enticott, P.G., Kennedy, H., Rinehart, N.J., Bradshaw, J.L., Tonge, B.J., Daskalakis, Z.J., et al. (2013). Interpersonal motor resonance in autism spectrum disorder: Evidence against a global “mirror system” deficit. Frontiers in Human Neuroscience, 7, 1–8.
- Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during action observation: A magnetic stimulation study. Journal of Neurophysiology, 73(6), 2608–2611.
- Fan, Y.T., Decety, J., Yang, C.-Y., Liu, J.-L., & Cheng, Y. (2010). Unbroken mirror neurons in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 51, 981–988.
- Filimon, F., Nelson, J.D., Hagler, D.J., & Sereno, M.I. (2007). Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery. NeuroImage, 37(4), 1315–1328.
- Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119(2), 593–609.
- Gallese, V., Fogassi, L., Fadiga, L., & Rizzolatti, G. (2001). Action representation and the inferior parietal lobule. In W. Prinz & B. Hommel (Ed.), Common mechanisms in perception and action: Attention and performance (pp. 334–355). Oxford: Oxford University Press.
- Gallese, V., Gernsbacher, M.A., Heyes, C., Hickok, G., & Iacoboni, M. (2011). Mirror neuron forum. Perspectives on Psychological Science, 6(4), 369–407.
- Genovese, C.R., Lazar, N.A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870–878.
- Ghaziuddin, M., & Butler, E. (1998). Clumsiness in autism and asperger syndrome: A further report. Journal of Intellectual Disability Research, 42(1), 43–48.
- Grafton, S.T., Arbib, M.A., Fadiga, L., & Rizzolatti, G. (1996). Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination. Experimental Brain Research. 112(1), 103–111.
- Green, D., Baird, G., Barnett, A.L., Henderson, L., Huber, J., & Henderson, S.E. (2002). The severity and nature of motor impairment in asperger's syndrome: A comparison with specific developmental disorder of motor function. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 43(5), 655–668.
- Grèzes, J., Armony, J.L., Rowe, J., & Passingham, R.E. (2003). Activations related to “mirror” and “canonical” neurones in the human brain: An fMRI study. Neuroimage, 18(4), 928–937.
- Grèzes, J., Costes, N., & Decety, J. (1999). The effects of learning and intention on the neural network involved in the perception of meaningless actions. Brain, 122 (Pt 10), 1875–1887.
- Grèzes, J., Wicker, B., Berthoz, S., & de Gelder, B. (2009). A failure to grasp the affective meaning of actions in autism spectrum disorder subjects. Neuropsychologia, 47(8–9), 1816–1825.
- Hamilton, A.F.C., & Grafton, S.T. (2006). Goal representation in human anterior intraparietal sulcus. The Journal of Neuroscience, 26(4), 1133–1137.
- Hamilton, A.F.C., & Grafton, S.T. (2007). The motor hierarchy: From kinematics to goals and intentions. In P. Haggard, Y. Rossetti, & M. Kawato (Eds.), Sensorimotor foundations of higher cognition: Attention and performance (pp. 381–408), Vol. 22. Oxford, UK: Oxford University Press.
- Hétu, S., Mercier, C., Eugène, F., Michon, P.E., & Jackson, P.L. (2011). Modulation of brain activity during action observation: Influence of perspective, transitivity and meaningfulness. PloS One, 6(9), e24728.
- Hickok, G. (2009). Eight problems for the mirror neuron theory of action understanding in monkeys and humans. Journal of Cognitive Neuroscience, 21(7), 1229–1243.
- Hobson, R.P., & Lee, A. (1999). Imitation and identification in autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 40(4), 649–659.
- Iacoboni, M. (2009). Imitation, empathy, and mirror neurons. Annual Review of Psychology, 60, 653–670.
- Iacoboni, M., & Dapretto, M. (2006). The mirror neuron system and the consequences of its dysfunction. Nature Reviews. Neuroscience, 7(12), 942–951.
- Iacoboni, M., Woods, R.P., Brass, M., Bekkering, H., Mazziotta, J.C., & Rizzolatti, G. (1999). Cortical mechanisms of human imitation. Science, 286(5449), 2526–2528.
- Kilner, J.M., Neal, A., Weiskopf, N., Friston, K.J., & Frith, C.D. (2009). Evidence of mirror neurons in human inferior frontal gyrus. The Journal of Neuroscience, 29(32), 10153–10159
- Koski, L., Wohlschläger, A., Bekkering, H., Woods, R.P., Dubeau, M.-C., Mazziotta, J.C., et. al. (2002). Modulation of motor and premotor activity during imitation of target-directed actions. Cerebral Cortex, 12(8), 847–855.
- Kraskov, A., Dancause, N., Quallo, M.M., Shepherd, S., & Lemon, R.N. (2009). Corticospinal neurons in macaque ventral premotor cortex with mirror properties: A potential mechanism for action suppression? Neuron, 64(6), 922–930.
- Lenroot, R.K., & Giedd, J.N. (2006). Brain development in children and adolescents: Insights from anatomical magnetic resonance imaging. Neuroscience and Biobehavioral Reviews, 30(6), 718–729.
- Liew, S.L., Han, S., & Aziz-Zadeh, L. (2011). Familiarity modulates mirror neuron and mentalizing regions during intention understanding. Human Brain Mapping, 32(11), 1986–1997.
- Lord, C., Risi, S., Lambrecht, L., Cook, E.H., 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.
- Lui, F., Buccino, G., Duzzi, D., Benuzzi, F., Crisi, G., Baraldi, P., et al. (2008). Neural substrates for observing and imagining non-object-directed actions. Social Neuroscience, 3(3–4), 261–275.
- Maeda, F., Kleiner-Fisman, G., & Pascual-Leone, A. (2002). Motor facilitation while observing hand actions: Specificity of the effect and role of observer's orientation. Journal of Neurophysiology, 87(3), 1329–1335.
- Marsh, L.E., & Hamilton, A.F.C. (2011). Dissociation of mirroring and mentalising systems in autism. NeuroImage, 56(3), 1511–1519.
- Martineau, J., Andersson, F., Barthélémy, C., Cottier, J.-P., & Destrieux, C. (2010). Atypical activation of the mirror neuron system during perception of hand motion in autism. Brain Research, 1320, 168–175.
- Menz, M.M., McNamara, A., Klemen, J., & Binkofski, F. (2009). Dissociating networks of imitation. Human Brain Mapping, 30(10), 3339–3350.
- Molenberghs, P., Cunnington, R., & Mattingley, J.B. (2012). Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies. Neuroscience and Biobehavioral Reviews, 36, 341–349.
- Montgomery, K.J., Isenberg, N., & Haxby, J.V. (2007). Communicative hand gestures and object-directed hand movements activated the mirror neuron system. Social Cognitive and Affective Neuroscience, 2(2), 114–122.
- Mukamel, R., Ekstrom, A.D., Kaplan, J., Iacoboni, M., & Fried, I. (2010). Single-neuron responses in humans during execution and observation of actions. Current Biology, 20(8), 750–756.
- Muthukumaraswamy, S.D., Johnson, B.W., & McNair, N.A. (2004). Mu rhythm modulation during observation of an object-directed grasp. Cognitive Brain Research, 19(2), 195–201.
- Newman-Norlund, R., van Schie, H.T., van Hoek, M.E., Cuijpers, R.H., & Bekkering, H. (2010). The role of inferior frontal and parietal areas in differentiating meaningful and meaningless object-directed actions. Brain Research, 1315, 63–74.
- Oberman, L.M., & Ramachandran, V.S. (2007). The simulating social mind: The role of the mirror neuron system and simulation in the social and communicative deficits of autism spectrum disorders. Psychological Bulletin, 133(2), 310–327.
- Oosterhof, N.N., Wiggett, A.J., Diedrichsen, J., Tipper, S.P., & Downing, P.E. (2010). Surface-based information mapping reveals crossmodal vision-action representations in human parietal and occipitotemporal cortex. Journal of Neurophysiology, 104(2), 1077–1089.
- Pelphrey, K.A., Morris, J.P., & McCarthy, G. (2004). Grasping the intentions of others: The perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. Journal of Cognitive Neuroscience, 16(10), 1706–1716.
- Raymaekers, R., Wiersema, J.R., & Roeyers, H. (2009). EEG study of the mirror neuron system in children with high-functioning autism. Brain Research, 1304, 113–121.
- Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169–192.
- Rizzolatti, G., & Fabbri-Destro, M. (2010). Mirror neurons: From discovery to autism. Experimental Brain Research, 200, 223–237.
- Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, F. (1996). Premotor cortex and the recognition of motor actions. Cognitive Brain Research, 3(2), 131–141.
- Rizzolatti, G., Fadiga, L., Matelli, M., Bettinardi, V., Paulesu, E., Perani, D., et al. (1996). Localization of grasp representations in humans by PET: 1. Observation versus execution. Experimental Brain Research, 111, 246–252.
- Rizzolatti, G., & Fogassi, L. (2014). The mirror mechanism: Recent findings and perspectives. Philosophical Transactions of the Royal Society B, 369, 20130420.
- Rizzolatti, G., Fogassi, L., & Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience, 2(9), 661–670.
- Rizzolatti, G., & Sinigaglia, C. (2010). The functional role of the parieto-frontal mirror circuit: Interpretations and misinterpretations. Nature Reviews Neuroscience, 11(4), 264–274.
- Rogers, S.J., Bennetto, L., McEvoy, R., & Pennington, B.F. (1996). Imitation and pantomime in high-functioning adolescents with autism spectrum disorders. Child Development, 67(5), 2060–2067.
- Rogers, S.J., & Williams, J.H. (2006). Imitation in autism: Findings and controversies. In S.J. Rogers & J.H. Williams (Eds.), Imitation and the social mind (pp. 277–309). NY: The Guilford Press.
- Rozzi, S., Ferrari, P.F., Bonini, L., Rizzolatti, G., & Fogassi, L. (2008). Functional organization of inferior parietal lobule convexity in the macaque monkey: Electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. The European Journal of Neuroscience, 28(8), 1569–1588.
- Rutter, M., Bailey, A., & Lord, C. (2003). SCQ: Social communication questionnaire. Los Angeles, CA: Western Psychological Services.
- Shaw, D.J., Grosbras, M.H., Leonard, G., Pike, G.B., & Paus, T. (2012). Development of the action observation network during early adolescence: A longitudinal study. Social Cognitive and Affective Neuroscience, 7(1), 64–80.
- Smith, I.M., & Bryson, S.E. (1994). Imitation and action in autism: A critical review. Psychological Bulletin, 116(2), 259–273.
- Smith, I.M., & Bryson, S.E. (2007). Gesture imitation in autism. II. Symbolic gestures and pantomimed object use. Cognitive Neuropsychology, 24(7), 679–700.
- Stone, W.L., Ousley, O.Y., & Littleford, C.D. (1997). Motor imitation in young children with autism: What's the object? Journal of Abnormal Child Psychology, 25(6), 475–485.
- Tanaka, S., & Inui, T. (2002). Cortical involvement for action imitation of hand/arm postures versus finger configurations: An fMRI study. Neuroreport, 13(13), 1599–1602.
- Tunik, E., Rice, N.J., Hamilton, A., & Grafton, S.T. (2007). Beyond grasping: Representation of action in human anterior intraparietal sulcus. Neuroimage, 36 Suppl 2, T77–T86.
- Turella, L., Tubaldi, F., Erb, M., Grodd, W., & Castiello, U. (2012). Object presence modulates activity within the somatosensory component of the action observation network. Cerebral Cortex, 22(3), 668–679.
- Umiltà, M.A., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., et al. (2001). I know what you are doing: A neurophysiological study. Neuron, 31, 155–165.
- Vanvuchelen, M., Roeyers, H., & De Weerdt, W. (2007). Nature of motor imitation problems in school-aged males with autism: How congruent are the error types? Developmental Medicine & Child Neurology, 49(1), 6–12.
- Villarreal, M., Fridman, E.A., Amengual, A., Falasco, G., Gerscovich, E.R., Ulloa, E.R., et al. (2008). The neural substrate of gesture recognition. Neuropsychologia, 46(9), 2371–2382.
- Vivanti, G., & Hamilton, A. (2014). Imitation in autism spectrum disorders. In F.R. Volkmar, P. Rhea, S.J. Rogers, & K.A. Pelphrey (Eds.), Handbook of autism and pervasive developmental disorders ( 4th ed.), Vol 1. Diagnosis, development and brain mechanisms (pp. 278–301). New York: Wiley.
-
Wiggins, L.D.,
Bakeman, R.,
Adamson, L.B., &
Robins, D.L. (2007). The utility of the social communication questionnaire in screening for autism in children referred for early intervention. Focus on Autism and Other Developmental Disabilities, 22(1), 33–38.
10.1177/10883576070220010401 Google Scholar
- Williams, J.H.G., Whiten, A., & Singh, T. (2004). A systematic review of action imitation in autistic spectrum disorder. Journal of Autism and Developmental Disorders, 34(3), 285–299.
- Wilson, B.N., Crawford, S.G., Green, D., Roberts, G., Aylott, A., & Kaplan, B.J. (2009). Psychometric properties of the revised developmental coordination disorder questionnaire. Physical and Occupational Therapy in Pediatrics, 29(2), 182–202.
- Zachor, D.A., Ilanit, T., & Itzchak, E.B. (2010). Autism severity and motor abilities correlates of imitation situations in children with autism spectrum disorders. Research in Autism Spectrum Disorders, 4(3), 438–443.
Citing Literature
