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Learning by observation in children with autism spectrum disorder

Published online by Cambridge University Press:  10 January 2014

F. Foti ,
L. Mazzone ,
D. Menghini ,
L. De Peppo ,
F. Federico ,
V. Postorino ,
E. Baumgartner ,
G. Valeri ,
L. Petrosini  and
S. Vicari
F. Foti*
Affiliation:
Department of Psychology, Sapienza University of Rome, Italy IRCCS Fondazione Santa Lucia, Rome, Italy
L. Mazzone
Affiliation:
Child Neuropsychiatry Unit, Department of Neuroscience, Bambino Gesù Children's Hospital, Rome, Italy
D. Menghini
Affiliation:
Child Neuropsychiatry Unit, Department of Neuroscience, Bambino Gesù Children's Hospital, Rome, Italy
L. De Peppo
Affiliation:
Child Neuropsychiatry Unit, Department of Neuroscience, Bambino Gesù Children's Hospital, Rome, Italy
F. Federico
Affiliation:
Department of Developmental and Social Psychology, Sapienza University of Rome, Italy
V. Postorino
Affiliation:
Child Neuropsychiatry Unit, Department of Neuroscience, Bambino Gesù Children's Hospital, Rome, Italy
E. Baumgartner
Affiliation:
Department of Developmental and Social Psychology, Sapienza University of Rome, Italy
G. Valeri
Affiliation:
Child Neuropsychiatry Unit, Department of Neuroscience, Bambino Gesù Children's Hospital, Rome, Italy
L. Petrosini
Affiliation:
Department of Psychology, Sapienza University of Rome, Italy IRCCS Fondazione Santa Lucia, Rome, Italy
S. Vicari
Affiliation:
Child Neuropsychiatry Unit, Department of Neuroscience, Bambino Gesù Children's Hospital, Rome, Italy
*
* Address for correspondence: F. Foti, Ph.D., Department of Psychology, Sapienza University of Rome, Via dei Marsi 78, 00185 Rome, Italy. (Email: [email protected])
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Abstract

Background

Observing another person performing a complex action accelerates the observer's acquisition of the same action and limits the time-consuming process of learning by trial and error. Learning by observation requires specific skills such as attending, imitating and understanding contingencies. Individuals with autism spectrum disorder (ASD) exhibit deficits in these skills.

Method

The performance of 20 ASD children was compared with that of a group of typically developing (TD) children matched for chronological age (CA), IQ and gender on tasks of learning of a visuomotor sequence by observation or by trial and error. Acquiring the correct sequence involved three phases: a detection phase (DP), in which participants discovered the correct sequence and learned how to perform the task; an exercise phase (EP), in which they reproduced the sequence until performance was error free; and an automatization phase (AP), in which by repeating the error-free sequence they became accurate and speedy.

Results

In the DP, ASD children were impaired in detecting a sequence by trial and error only when the task was proposed as first, whereas they were as efficient as TD children in detecting a sequence by observation. In the EP, ASD children were as efficient as TD children. In the AP, ASD children were impaired in automatizing the sequence. Although the positive effect of learning by observation was evident, ASD children made a high number of imitative errors, indicating marked tendencies to hyperimitate.

Conclusions

These findings demonstrate the imitative abilities of ASD children although the presence of imitative errors indicates an impairment in the control of imitative behaviours.

Keywords

Autism spectrum disorderimitationobservational learningsequential learning
Type
Original Articles
Information
Psychological Medicine , Volume 44 , Issue 11 , August 2014 , pp. 2437 - 2447
Copyright
Copyright © Cambridge University Press 2014 

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References

Agam, Y, Joseph, RM, Barton, JJ, Manoach, DS (2010). Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders. NeuroImage 52, 336–347.CrossRefGoogle ScholarPubMed
Allen, G, Muller, RA, Courchesne, E (2004). Cerebellar function in autism: functional magnetic resonance image activation during a simple motor task. Biological Psychiatry 56, 269–278.Google Scholar
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association: Washington, DC.Google Scholar
Bailey, A, Luthert, P, Dean, A, Harding, B, Janota, I, Montgomery, M, Rutter, M, Lantos, P (1998). A clinicopathological study of autism. Brain 121, 889–905.Google Scholar
Bandura, A (1977). Social Learning Theory. Prentice Hall: Englewood Cliffs, NJ.Google Scholar
Beery, KE, Buktenica, NA (2000). The Beery–Buktenica Developmental Test of Visual-Motor Integration with Additional Tests of Visual Perception and Motor Coordination [Italian translation by C. Preda] . O.S. Organizzazioni Speciali: Florence.Google Scholar
Bernier, R, Dawson, G, Webb, S, Murias, M (2007). EEG mu rhythm and imitation impairments in individuals with autism spectrum disorder. Brain and Cognition 64, 228–237.Google Scholar
Biancardi, A, Stoppa, E (1997). The modified Bells Test: a proposal for the study of attention in childhood [in Italian]. Psichiatria dell'Infanzia e dell'Adolescenza 64, 73–84.Google Scholar
Bird, G, Heyes, C (2005). Effector-dependent learning by observation of a finger movement sequence. Journal of Experimental Psychology: Human Perception and Performance 31, 262–275.Google ScholarPubMed
Buccino, G, Binkofski, F, Fink, GR, Fadiga, L, Fogassi, L, Gallese, V, Seitz, RJ, Zilles, K, Rizzolatti, G, Freund, HJ (2001). Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. European Journal of Neuroscience 13, 400–404.Google Scholar
Chambers, CD, Bellgrove, MA, Gould, IC, English, T, Garavan, H, McNaught, E, Kamke, M, Mattingley, JB (2007). Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. Journal of Neurophysiology 98, 3638–3647.Google Scholar
Cheung, C, Chua, SE, Cheung, V, Khong, PL, Tai, KS, Wong, TK, Ho, TP, McAlonan, GM (2009). White matter fractional anisotrophy differences and correlates of diagnostic symptoms in autism. Journal of Child Psychology and Psychiatry 50, 1102–1112.Google Scholar
Clarke, HF, Robbins, TW, Roberts, AC (2008). Lesions of the medial striatum in monkeys produce perseverative impairments during reversal learning similar to those produced by lesions of the orbitofrontal cortex. Journal of Neuroscience 28, 10972–10982.Google Scholar
Cook, J, Barbalat, G, Blakemore, SJ (2012). Top-down modulation of the perception of other people in schizophrenia and autism. Frontiers in Human Neuroscience 6, 175.Google Scholar
Cook, J, Swapp, D, Pan, X, Bianchi-Berthouze, N, Blakemore, SJ (2013). Atypical interference effect of action observation in autism spectrum conditions. Psychological Medicine. Published online: 13 June 2013 . doi:10.1017/S0033291713001335.Google Scholar
Corbett, BA, Constantine, LJ, Hendren, R, Rocke, D, Ozonoff, S (2009). Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development. Psychiatry Research 166, 210–222.Google Scholar
Dapretto, M, Davies, MS, Pfeifer, JH, Scott, AA, Sigman, M, Bookheimer, SY, Iacoboni, M (2006). Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience 9, 28–30.Google Scholar
Donnelly, JI, Luyben, PD, Zan, CS (2009). Increasing eye contact toward learning materials in a toddler with autism. Journal of Prevention and Intervention in the Community 37, 170–176.Google Scholar
Ersche, KD, Roiser, JP, Abbott, S, Craig, KJ, Muller, U, Suckling, J, Ooi, C, Shabbir, SS, Clark, L, Sahakian, BJ, Fineberg, NA, Merlo-Pich, EV, Robbins, TW, Bullmore, ET (2011). Response perseveration in stimulant dependence is associated with striatal dysfunction and can be ameliorated by a D(2/3) receptor agonist. Biological Psychiatry 70, 754–762.Google Scholar
Esseily, R, Nadel, J, Fagard, J (2010). Object retrieval through observational learning in 8- to 18-month-old infants. Infant Behavior and Development 33, 695–699.Google Scholar
Falter, CM, Plaisted, KC, Davis, G (2008). Visuo-spatial processing in autism – testing the predictions of extreme male brain theory. Journal of Autism and Developmental Disorder 38, 507–515.Google Scholar
Foti, F, Menghini, D, Mandolesi, L, Federico, F, Vicari, S, Petrosini, L (2013). Learning by observation: insights from Williams syndrome. PLoS One 8, e53782.Google Scholar
Gallese, V, Goldman, A (1998). Mirror neurons and the simulation theory of mind-reading. Trends in Cognitive Sciences 2, 493–501.CrossRefGoogle ScholarPubMed
Grandin, T (1995). Thinking in Pictures. Vintage Press Random House: New York.Google Scholar
Grandin, T (2009). How does visual thinking work in the mind of a person with autism? Philosophical Transactions of the Royal Society of London . Series B, Biological Sciences 364, 1437–1442.Google Scholar
Hamilton, AF (2008). Emulation and mimicry for social interaction: a theoretical approach to imitation in autism. Quarterly Journal of Experimental Psychology 61, 101–115.Google Scholar
Hamilton, AF, Brindley, RM, Frith, U (2007). Imitation and action understanding in autistic spectrum disorders: how valid is the hypothesis of a deficit in the mirror neuron system? Neuropsychologia 45, 1859–1868.Google Scholar
Haznedar, MM, Buchsbaum, MS, Hazlett, EA, LiCalzi, EM, Cartwright, C, Hollander, E (2006). Volumetric analysis and three-dimensional glucose metabolic mapping of the striatum and thalamus in patients with autism spectrum disorders. American Journal of Psychiatry 163, 1252–1263.Google Scholar
Herbert, J, Gross, J, Hayne, H (2006). Age-related changes in deferred imitation between 6 and 9 months of age. Infant Behaviour and Development 29, 136–139.Google Scholar
Hill, EL (2004). Executive dysfunction in autism. Trends in Cognitive Sciences 8, 26–32.Google Scholar
Hollander, E, Anagnostou, E, Chaplin, W, Esposito, K, Haznedar, MM, Licalzi, E, Wasserman, S, Soorya, L, Buchsbaum, M (2005). Striatal volume on magnetic resonance imaging and repetitive behaviors in autism. Biological Psychiatry 58, 226–232.Google Scholar
Iacoboni, M, Woods, RP, Brass, M, Bekkering, H, Mazziotta, JC, Rizzolatti, G (1999). Cortical mechanisms of human imitation. Science 286, 2526–2528.CrossRefGoogle ScholarPubMed
Just, MA, Cherkassky, VL, Keller, TA, Kana, RK, Minshew, NJ (2007). Functional and anatomical cortical underconnectivity in autism: evidence from an FMRI study of an executive function task and corpus callosum morphometry. Cerebral Cortex 17, 951–961.CrossRefGoogle ScholarPubMed
Kana, R, Wadsworth, H, Travers, B (2011). A systems level analysis of the mirror neuron hypothesis and imitation impairments in autism spectrum disorders. Neuroscience and Biobehavioral Reviews 35, 894–902.Google Scholar
Klin, AK, Sparrow, SS, de Bildt, A, Cicchetti, DV, Cohen, DJ, Volkmar, FR (1999). A normed study of face recognition in autism and related disorders. Journal of Autism and Developmental Disorders 29, 499–508.Google Scholar
Kokkinakki, T, Kugiumutzakis, G (2000). Basic aspects of vocal imitation in infant-parent interaction during the first 6 months. Journal of Reproductive and Infant Psychology 18, 173–187.Google Scholar
Kunda, M, Goel, AK (2011). Thinking in Pictures as a cognitive account of autism. Journal of Autism and Developmental Disorders 41, 1157–1177.Google Scholar
Langen, M, Schnack, HG, Nederveen, H, Bos, D, Lahuis, BE, de Jonge, MV, van Engeland, H, Durston, S (2009). Changes in the developmental trajectories of striatum in autism. Biological Psychiatry 66, 327–333.Google Scholar
Leekam, SR, Hunnisett, E, Moore, C (1998). Targets and cues: gaze-following in children with autism. Journal of Child Psychology and Psychiatry 39, 951–962.CrossRefGoogle ScholarPubMed
Leighton, J, Bird, G, Charman, T, Heyes, C (2008). Weak imitative performance is not due to a functional ‘mirroring’ deficit in adults with autism spectrum disorders. Neuropsychologia 46, 1041–1049.Google Scholar
Lord, C, Rutter, M, Di Lovore, PC, Risi, S (2005). Autism Diagnostic Observation Schedule. Organizzazioni Speciali: Florence, Italy.Google Scholar
Luna, B, Minshew, NJ, Garver, KE, Lazar, NA, Thulborn, KR, Eddy, WF, Sweeney, JA (2002). Neocortical system abnormalities in autism: an fMRI study of spatial working memory. Neurology 59, 834–840.Google Scholar
Marsh, L, Pearson, A, Ropar, D, Hamilton, A (2013). Children with autism do not overimitate. Current Biology 23, R266–R268.Google Scholar
Martin, LA, Goldowitz, D, Mittleman, G (2010). Repetitive behavior and increased activity in mice with Purkinje cell loss: a model for understanding the role of cerebellar pathology in autism. European Journal of Neuroscience 31, 544–555.Google Scholar
Martineau, J, Andersson, F, Barthelemy, C, Cottier, JP, Destrieux, C (2010). Atypical activation of the mirror neuron system during perception of hand motion in autism. Brain Research 1320, 168–175.Google Scholar
Meltzoff, AN, Andrew, N (1995). Understanding the intentions of others: re-enactment of intended acts by 18-month-old children. Developmental Psychology 31, 838–850.Google Scholar
Meltzoff, AN, Moore, MK (1997). Imitation of facial and manual gestures by human neonates. Science 198, 75–78.Google Scholar
Meltzoff, AN, Decety, J (2003). What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 358, 491–500.Google Scholar
Meltzoff, AN, Kuhl, PK, Movellan, J, Sejnowski, TJ (2009). Foundations for a new science of learning. Science 325, 284–288.Google Scholar
Menghini, D, Hagberg, GE, Caltagirone, C, Petrosini, L, Vicari, S (2006). Implicit learning deficits in dyslexic adults: an fMRI study. NeuroImage 33, 1218–1226.Google Scholar
Menghini, D, Vicari, S, Mandolesi, L, Petrosini, L (2011). Is learning by observation impaired in children with dyslexia? Neuropsychologia 49, 1996–2003.Google Scholar
Middleton, FA, Strick, PL (2000). Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Research. Brain Research Reviews 31, 236–250.Google Scholar
Mottron, L, Belleville, S, Ménard, E (1999). Local bias in autistic subjects as evidenced by graphic tasks: perceptual hierarchization or working memory deficit? Journal of Child Psychology and Psychiatry 40, 743–755.Google Scholar
Mundy, P, Crowson, M (1997). Joint attention and early social communication: implication for research on intervention with autism. Journal of Autism and Developmental Disorders 27, 653–676.Google Scholar
Nadel, J (2002). Imitation and imitation recognition: functional use in preverbal infants and nonverbal children with autism. The Imitative Mind: Development, Evolution, and Brain Bases . In The Imitative Mind (ed. Meltzoff, A. and Prinz, W.), pp. 42–62. Cambridge University Press: Cambridge.Google Scholar
Nadel, J, Aouka, N, Coulon, N, Gras-Vincendon, A, Canet, P, Fagard, J, Bursztejn, C (2011). Yes they can! An approach to observational learning in low-functioning children with autism. Autism 15, 421–435.Google Scholar
Nadel, J, Butterworth, G (1998). Imitation in Infancy. Cambridge University Press: Cambridge.Google Scholar
Neuhaus, E, Beauchaine, TP, Bernier, R (2010). Neurobiological correlates of social functioning in autism. Clinical Psychology Review 30, 733–748.Google Scholar
Nobile, M, Alberti, B, Zuddas, A (2007). Conners' Rating Scales – Revised 2007 [Italian adaptation] . Giunti O.S. Organizzazioni Speciali: Florence.Google Scholar
O'Riordan, MA, Plaisted, KC, Driver, J, Baron-Cohen, S (2001). Superior visual search in autism. Journal of Experimental Psychology: Human Perception and Performance 27, 719–730.Google Scholar
Ozonoff, S, Strayer, DL (2001). Further evidence of intact working memory in autism. Journal of Autism and Developmental Disorders 31, 257–263.Google Scholar
Pellicano, E (2012). The development of executive function in autism. Autism Research and Treatment 2012, 146132–146140.Google Scholar
Petrosini, L (2007). ‘Do what I do’ and ‘do how I do’: different components of imitative learning are mediated by different neural structures. Neuroscientist 13, 335–348.Google Scholar
Ramachandran, V, Oberman, L (2006). Broken mirrors: a theory of autism. Scientific American 295, 62–69.Google Scholar
Rizzolatti, G, Craighero, L (2004). The mirror-neuron system. Annual Review of Neuroscience 27, 169–192.Google Scholar
Robinson, S, Goddard, L, Dritschel, B, Wisley, M, Howlin, P (2009). Executive functions in children with autism spectrum disorders. Brain and Cognition 71, 362–368.Google Scholar
Rogers, SJ, Pennington, BF (1991). A theoretical approach to the deficits in infantile autism. Development and Psychopathology 3, 137–162.Google Scholar
Rojas, DC, Peterson, E, Winterrowd, E, Reite, ML, Rogers, SJ, Tregellas, JR (2006). Regional gray matter volumetric changes in autism associated with social and repetitive behavior symptoms. BMC Psychiatry 6, 56.Google Scholar
Russell, J (1997). Autism as an Executive Disorder. Oxford University Press: New York.Google Scholar
Rutter, M (1974). The development of infantile autism. Psychological Medicine 4, 147–163.Google Scholar
Sears, LL, Vest, C, Mohamed, S, Bailey, J, Ranson, BJ, Piven, J (1999). An MRI study of the basal ganglia in autism. Progress in Neuro-psychopharmacology and Biological Psychiatry 23, 613–624.Google Scholar
Seidler, RD, Purushotham, A, Kim, SG, Ugurbil, K, Willingham, D, Ashe, J (2005). Neural correlates of encoding and expression in implicit sequence learning. Experimental Brain Research 165, 114–124.Google Scholar
Shah, A, Frith, U (1993). Why do autistic individuals show superior performance on the block design task? Journal of Child Psychology and Psychiatry 34, 1351–1364.CrossRefGoogle ScholarPubMed
Shic, F, Bradshaw, J, Klin, A, Scassellati, B, Chawarska, K (2011). Limited activity monitoring in toddlers with autism spectrum disorder. Brain Research 1380, 246–254.Google Scholar
Shih, P, Shen, M, Ottl, B, Keehn, B, Gaffrey, M, Müller, R (2010). Atypical network connectivity for imitation in autism spectrum disorder. Neuropsychologia 48, 2931–2939.Google Scholar
Silk, TJ, Rinehart, N, Bradshaw, JL, Tonge, B, Egan, G, O'Boyle, MW, Cunnington, R (2006). Visuospatial processing and the function of prefrontal-parietal networks in autism spectrum disorders: a functional MRI study. American Journal of Psychiatry 163, 1440–14443.Google Scholar
Soulières, I, Zeffiro, TA, Girard, ML, Mottron, L (2011). Enhanced mental image mapping in autism. Neuropsychologia 49, 848–857.Google Scholar
Southgate, V, Hamilton, AF (2008). Unbroken mirrors: challenging a theory of autism. Trends in Cognitive Sciences 12, 225–229.Google Scholar
Spengler, S, von Cramon, DY, Brass, M (2010). Resisting motor mimicry: control of imitation involves processes central to social cognition in patients with frontal and temporo-parietal lesions. Social Neuroscience 5, 401–416.Google Scholar
Stuss, DT, Knight, RT (2002). Principles of Frontal Lobe Function. Oxford University Press: Oxford.Google Scholar
Swick, D, Ashley, V, Turken, U (2011). Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. NeuroImage 56, 1655–1665.Google Scholar
Taylor, BA, DeQuinzio, JA (2012). Observational learning and children with autism. Behavior Modification 36, 341–360.Google Scholar
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, R84–R85.Google Scholar
Torriero, S, Oliveri, M, Koch, G, Lo Gerfo, E, Salerno, S, Ferlazzo, F, Caltagirone, C, Petrosini, L (2011). Changes in cerebello-motor connectivity during procedural learning by actual execution and observation. Journal of Cognitive Neuroscience 23, 338–348.Google Scholar
Tsai, PT, Hull, C, Chu, Y, Greene-Colozzi, E, Sadowski, AR, Leech, JM, Steinberg, J, Crawley, JN, Regehr, WG, Sahin, M (2012). Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature 488, 647–651.CrossRefGoogle ScholarPubMed
Verhoeven, JS, De Cock, P, Lagae, L, Sunaert, S (2010). Neuroimaging of autism. Neuroradiology 52, 3–14.Google Scholar
Wechsler, D (1991). Manual for the Wechsler Intelligence Scale for Children – 3rd Edition. The Psychological Corporation: San Antonio, TX.Google Scholar
Williams, JH, Whiten, A, Singh, T (2004). A systematic review of action imitation in autistic spectrum disorder. Journal of Autism and Developmental Disorders 34, 285–299.Google Scholar
Williams, JH, Whiten, A, Suddendorf, T, Perrett, DI (2001). Imitation, mirror neurons and autism. Neuroscience and Biobehavioural Reviews 25, 287–295.Google Scholar