Journal of Autism and Developmental Disorders

, Volume 45, Issue 3, pp 805–815 | Cite as

Cognitive Set Shifting Deficits and Their Relationship to Repetitive Behaviors in Autism Spectrum Disorder

  • Haylie L. Miller
  • Michael E. Ragozzino
  • Edwin H. Cook
  • John A. Sweeney
  • Matthew W. Mosconi
Original Paper

Abstract

The neurocognitive impairments associated with restricted and repetitive behaviors (RRBs) in autism spectrum disorder (ASD) are not yet clear. Prior studies indicate that individuals with ASD show reduced cognitive flexibility, which could reflect difficulty shifting from a previously learned response pattern or a failure to maintain a new response set. We examined different error types on a test of set-shifting completed by 60 individuals with ASD and 55 age- and nonverbal IQ-matched controls. Individuals with ASD were able to initially shift sets, but they exhibited difficulty maintaining new response sets. Difficulty with set maintenance was related to increased severity of RRBs. General difficulty maintaining new response sets and a heightened tendency to revert to old preferences may contribute to RRBs.

Keywords

Cognitive flexibility Insistence on sameness Repetitive behavior 

Supplementary material

10803_2014_2244_MOESM1_ESM.doc (98 kb)
Supplementary material 1 (DOC 95 kb)

References

  1. Agam, Y., Joseph, R. M., Barton, J. J. S., & Manoach, D. S. (2010). Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders. NeuroImage, 52, 336–347.CrossRefPubMedCentralPubMedGoogle Scholar
  2. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). Washington, DC: American Psychiatric Publishing.Google Scholar
  3. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.CrossRefGoogle Scholar
  4. Amodeo, D. A., Jones, J. H., Sweeney, J. A., & Ragozzino, M. E. (2014). Risperidone and the 5-HT2a receptor antagonist M100907 improve probabilistic reversal learning in BTBR T + tf/J mice. Autism Research, online advance publication. doi: 10.1002/aur1395.
  5. Baker, P. M., Thompson, J. L., Sweeney, J. A., & Ragozzino, M. E. (2011). Differential effects of 5-HT2A and 5-HT2C receptor blockade on strategy-switching. Behavioural Brain Research, 219(1), 123–131.CrossRefPubMedCentralPubMedGoogle Scholar
  6. Barceló, F., & Knight, R. T. (2002). Both random and perseverative errors underlie WCST deficits in prefrontal patients. Neuropsychologia, 40, 349–356.CrossRefPubMedGoogle Scholar
  7. Bishop, D. V. M., & Norbury, C. F. (2005). Executive functions in children with communication impairments, in relation to autistic symptomatology. Autism, 9(1), 7–43.CrossRefPubMedGoogle Scholar
  8. Bissonette, G. B., Martins, G. J., Franz, T. M., Harper, E. S., Schoenbaum, G., & Powell, E. M. (2008). Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. Journal of Neuroscience, 28(44), 11124–11130.CrossRefPubMedCentralPubMedGoogle Scholar
  9. Brown, H. D., Amodeo, D. A., Sweeney, J. A., & Ragozzino, M. E. (2012). The selective serotonin reuptake inhibitor, escitalopram, enhances inhibition of prepotent responding and spatial reversal learning. Journal of Psychopharmacology, 26(11), 1443–1455.CrossRefPubMedCentralPubMedGoogle Scholar
  10. Brown, H. D., Baker, P. M., & Ragozzino, M. E. (2010). The parafascicular thalamic nucleus concomitantly influences behavioral flexibility and dorsomedial striatal acetylcholine output in rats. Journal of Neuroscience, 30(43), 14390–14398.CrossRefPubMedCentralPubMedGoogle Scholar
  11. Cody, H., Pelphrey, K., & Piven, J. (2002). Structural and functional magnetic resonance imaging of autism. International Journal of Developmental Neuroscience, 20(3–5), 421–438.CrossRefPubMedGoogle Scholar
  12. Cody-Hazlett, H., Poe, M. D., Gerig, G., Gimpel-Smith, R., & Piven, J. (2006). Cortical gray and white brain tissue volume in adolescents and adults with autsm. Biological Psychiatry, 59, 1–6.CrossRefGoogle Scholar
  13. Corbett, B. A., Constantine, L. J., 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(2–3), 201–222.Google Scholar
  14. Cuccaro, M. L., Shao, Y., Grubber, J., Slifer, M., Wolpert, C. M., Donnelly, S. L., et al. (2003). Factor analysis of restricted and repetitive behaviors in autism using the Autism Diagnostic Interview-R. Child Psychiatry and Human Development, 34(1), 3–17.CrossRefPubMedGoogle Scholar
  15. D’Cruz, A. M., Mosconi, M. W., Ragozzino, M. E., Pavuluri, M., & Sweeney, J. A. (2011). Human reversal learning under conditions of certain versus uncertain outcomes. NeuroImage, 56, 315–322.CrossRefPubMedCentralPubMedGoogle Scholar
  16. D’Cruz, A., Ragozzino, M. E., Mosconi, M. W., Shrestha, S., Cook, E. H., & Sweeney, J. A. (2013). Reduced behavioral flexibility is related to “Insistence on Sameness” in Autism Spectrum Disorders. Neuropsychology, 27(2), 152–160.CrossRefPubMedCentralPubMedGoogle Scholar
  17. Deshpande, G., Libero, L. E., Sreenivasan, R., Deshpande, H. D., & Kana, R. K. (2013). Identification of neural connectivity signatures of autism using machine learning. Frontiers in Human Neuroscience. doi:10.3389/fnhum.2013.00670.PubMedCentralPubMedGoogle Scholar
  18. Dias, R., Robbins, T. W., & Roberts, A. C. (1997). Dissociable forms of inhibitory control within prefrontal cortex with an analogue of the Wisconsin Card Sort Test: Restriction to novel situations and independence from ‘on-line’ processing. Journal of Neuroscience, 17, 9285–9297.PubMedGoogle Scholar
  19. Elliot, C. D. (2007). Differential Ability Scales-II (DAS-II). San Antonio, TX: Pearson Clinical.Google Scholar
  20. Figueroa, I. J., & Youmans, R. Y. (2013). Failure to maintain set: A measure of distractibility or cognitive flexibility? In: Proceedings of the 57th annual human factors and ergonomics society.Google Scholar
  21. Floresco, S. B., Ghods-Sharifi, S., Vexelman, C., & Tse, M. T. (2006). Dissociable roles for the nucleus accumbens core and shell in regulating set shifting. Journal of Neuroscience, 26, 2449–2457.CrossRefPubMedGoogle Scholar
  22. Gastambide, F., Cotel, M. C., Gilmour, G., O’Neill, M. J., Robbins, T. W., & Tricklebank, M. D. (2012). Selective remediation of reversal learning deficits in the neurodevelopmental MAM model of schizophrenia by a novel mGlu5 positive allosteric modulator. Neuropsychopharmacology, 37(4), 1057–1066.CrossRefPubMedCentralPubMedGoogle Scholar
  23. Geurts, H. M., Corbett, B., & Solomon, M. (2009). The paradox of cognitive flexibility in autism. Trends in Cognitive Science, 13(2), 74–82.CrossRefGoogle Scholar
  24. Goldberg, M. C., Mostofsky, S. H., Cutting, L. E., Mahone, E. M., Astor, B. C., Denckla, M. B., et al. (2005). Subtle executive impairment in children with autism and children with ADHD. Journal of Autism and Developmental Disorders, 35(3), 279–293.CrossRefPubMedGoogle Scholar
  25. Gordon, C. T. (2000). Commentary: Considerations on the pharmacological treatment of compulsions and stereotypies with serotonin reuptake inhibitors in pervasive developmental disorders. Journal of Autism and Developmental Disorders, 30, 437–438.CrossRefPubMedGoogle Scholar
  26. Grant, D. A., & Berg, E. A. (1948). A behavioral analysis of degree of reinforcement and ease of shifting to new responses in a Weigl-type card sorting problem. Journal of Experimental Psychology, 34, 404–411.CrossRefGoogle Scholar
  27. Heaton, R. K., Chelune, G. J., Talley, J. L., Kay, G. G., & Curtiss, G. (1993). Wisconsin card sorting test manual: Revised and expanded. Odessa, FL: Psychological Assessment Resources.Google Scholar
  28. Kaland, N., Smith, L., & Mortensen, E. L. (2008). Brief report: Cognitive flexibility and focused attention in children and adolescents with Asperger syndrome and high-functioning autism as measured on the computerized version of the Wisconsin Card Sorting Test. Journal of Autism and Developmental Disorders, 38(6), 1161–1165.CrossRefPubMedGoogle Scholar
  29. Kenet, T., Orekhova, E. V., Bharadwaj, H., Shetty, N. R., Israeli, E., Lee, A. K., et al. (2012). Disconnectivity of the cortical ocular motor control network in autism spectrum disorders. NeuroImage, 61(4), 1226–1234.CrossRefPubMedCentralPubMedGoogle Scholar
  30. Kenworthy, L., Yerys, B. E., Anthony, L. G., & Wallace, G. L. (2008). Understanding executive control in autism spectrum disorders in the lab and in the real world. Neuropsychology Review, 18(4), 320–338.CrossRefPubMedCentralPubMedGoogle Scholar
  31. Kim, J., & Ragozzino, M. E. (2005). The involvement of the orbitofrontal cortex in learning under changing task contingencies. Neurobiology of Learning and Memory, 83, 125–133.CrossRefPubMedCentralPubMedGoogle Scholar
  32. Kuhlthau, K., Orlich, F., Hall, T. A., Sikora, D., Kovacs, E. A., Delahaye, J., et al. (2010). Health-related quality of life in children with autism spectrum disorders: Results from the Autism Treatment Network. Journal of Autism and Developmental Disorders, 40(6), 721–729.CrossRefPubMedGoogle Scholar
  33. Kurtz, M. M., Ragland, J. D., Moberg, P. J., & Gur, R. C. (2004). The Penn Conditional Exclusion Test: A new measure of executive-function with alternate forms. Archives of Clinical Neuropsychology, 19, 191–201.CrossRefPubMedGoogle Scholar
  34. Landa, R. J., & Goldberg, M. C. (2005). Language, social, and executive functions in high-functioning autism: A continuum of performance. Journal of Autism and Developmental Disorders, 35, 557–573.CrossRefPubMedGoogle Scholar
  35. Langen, M., Leemans, A., Johnston, P., Ecker, C., Daly, E., Murphy, C. M., et al. (2012). Fronto-striatal circuitry and inhibitory control in autism: Findings from diffusion tensor imaging tractography. Cortex, 48(2), 183–193.CrossRefPubMedGoogle Scholar
  36. LeCouteur, A., Rutter, M., Lord, C., & Rios, P. (1989). Autism diagnostic interview: A standardized investigator-based instrument. Journal of Autism and Developmental Disorders, 19(3), 363–387.CrossRefGoogle Scholar
  37. Leekam, S. R., Prior, M. R., & Uljarevic, M. (2011). Restricted and repetitive behaviors in autism spectrum disorders: A review of research in the last decade. Psychological Bulletin, 137(4), 562–593.CrossRefPubMedGoogle Scholar
  38. Liss, M., Fein, D., Allen, D., Dunn, M., Feinstein, C., Morris, R., et al. (2001). Executive functioning in high-functioning children with autism. Journal of Child Psychology and Psychiatry, 42(2), 261–270.CrossRefPubMedGoogle Scholar
  39. Lopez, B. R., Lincoln, A. J., Ozonoff, S., & Lai, Z. (2005). Examining the relationship between executive functions and restricted, repetitive symptoms of Autistic Disorder. Journal of Autism and Developmental Disorders, 35(4), 445–460.CrossRefPubMedGoogle Scholar
  40. Lord, C., Rutter, M., DiLavore, P. C., Risi, S., Gotham, K., & Bishop, S. (2012). Autism Diagnostic Observation Schedule, Second Edition (ADOS-2). Los Angeles, CA: Western Psychological Services.Google Scholar
  41. Lord, C., Rutter, M., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., et al. (1989). Autism Diagnostic Observation Schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185–212.CrossRefPubMedGoogle Scholar
  42. McAlonan, K., & Brown, V. J. (2003). Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behavior and Brain Research, 146, 97–103.CrossRefGoogle Scholar
  43. McAlonan, K., Cheung, V., Cheung, C., Suckling, J., Lam, G. Y., Tai, K. S., et al. (2005). Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain, 128(2), 268–276.CrossRefPubMedGoogle Scholar
  44. Minshew, N. J., Goldstein, G., & Siegel, D. J. (1997). Neuropsychologic functioning in autism: Profile of a complex information processing disorder. Journal of the International Neuropsychological Society, 3(4), 303–316.PubMedGoogle Scholar
  45. Mohler, E. G., Baker, P. M., Gannon, K. S., Jones, S. S., Shacham, S., Sweeney, J. A., et al. (2012). Psychopharmacology (Berl), 220(4), 687–696.CrossRefGoogle Scholar
  46. Mooney, E. L., Gray, K. M., Tonge, B. J., Sweeney, D. J., & Taffe, J. R. (2009). Factor analytic study of repetitive behaviours in young children with pervasive developmental disorders. Journal of Autism and Developmental Disorders, 39(5), 765–774.CrossRefPubMedGoogle Scholar
  47. Mosconi, M. W., Kay, M., Seidenfeld, A., Guter, S., Stanford, L. D., & Sweeney, J. A. (2009). Impaired cognitive control is associated with higher-order repetitive behaviors in autism spectrum disorders. Psychological Medicine, 39, 1355–1366.CrossRefGoogle Scholar
  48. Mosconi, M. W., Luna, B., Kay-Stacey, M., Nowinski, C. V., Rubin, L. H., Scudder, C., et al. (2013). Saccade adaptation abnormalities implicate dysfunction of cerebellar-dependent learning mechanisms in autism spectrum disorders (ASD). PLoS ONE, 8(5), e63709. doi:10.1371/journal.pone.0063709.CrossRefPubMedCentralPubMedGoogle Scholar
  49. Munson, J., Dawson, G., Sterling, L., Beauchaine, T., Zhou, A., Koehler, E., et al. (2008). Evidence for latent classes of IQ in young children with autism spectrum disorder. American Journal of Mental Retardation, 113(6), 439–452.CrossRefPubMedCentralPubMedGoogle Scholar
  50. Ozonoff, S. (1995). Reliability and validity of the Wisconsin Card Sorting Test in studies of autism. Neuropsychology, 9(4), 491–500.CrossRefGoogle Scholar
  51. Ozonoff, S., Cook, I., Coon, H., Dawson, G., Joseph, R., Klin, A., et al. (2004). Performance on CANTAB subtests sensitive to frontal lobe function in people with autistic disorder: Evidence from the CPEA network. Journal of Autism and Developmental Disorders, 34, 139–150.CrossRefPubMedGoogle Scholar
  52. Ozonoff, S., Rogers, S. J., & Pennington, B. F. (1991). Asperger’s syndrome: Evidence of an empirical distinction from high-functioning autism. Journal of Child Psychology and Psychiatry, 32, 1107–1122.CrossRefPubMedGoogle Scholar
  53. Palencia, C. A., & Ragozzino, M. E. (2004). The influence of NMDA receptors in the dorsomedial striatum on response reversal learning. Neurobiology of Learning and Memory, 82, 81–89.CrossRefPubMedGoogle Scholar
  54. Pellicano, E. (2007). Links between theory of mind and executive function in young children with autism: Clues to developmental primacy. Developmental Psychology, 43, 974–990.CrossRefPubMedGoogle Scholar
  55. Pellicano, E. (2010). The development of core cognitive skills in autism: A 3-year prospective study. Child Development, 81(5), 1400–1416.CrossRefPubMedGoogle Scholar
  56. Ragozzino, M. E. (2007). The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Annals of the New York Academy of Sciences, 1121, 355–375.CrossRefPubMedGoogle Scholar
  57. Ragozzino, M. E., & Choi, D. (2004). Dynamic changes in acetylcholine output in the medial striatum during place reversal learning. Learning and Memory, 11(1), 70–77.CrossRefPubMedCentralPubMedGoogle Scholar
  58. Ragozzino, M. E., Detrich, S., & Kesner, R. P. (1999). Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. Journal of Neuroscience, 19, 4585–4594.PubMedGoogle Scholar
  59. Ragozzino, M. E., Ragozzino, K. E., Mizumori, S. J., & Kesner, R. P. (2002). Role of the dorsomedial striatum in behavioral flexibility for response and visual cue discrimination learning. Behavioral Neuroscience, 116, 105–115.CrossRefPubMedCentralPubMedGoogle Scholar
  60. Ranier, G. (2007). Behavioral flexibility and the frontal lobe. Neuron, 53(3), 321–323.CrossRefGoogle Scholar
  61. Ravizza, S. M., Solomon, M., Ivry, R. B., & Carter, C. S. (2013). Restricted and repetitive behaviors in autism spectrum disorders: The relationship of attention and motor deficits. Development and Psychopathology, 25, 773–784.CrossRefPubMedGoogle Scholar
  62. Rinehart, N. J., Bradshaw, J. L., Brereton, A. V., & Tonge, B. J. (2002). Lateralization in individuals with high-functioning autism and Asperger’s disorder: A frontostriatal model. Journal of Autism and Developmental Disorders, 32(4), 321–332.CrossRefPubMedGoogle Scholar
  63. Rinehart, N. J., Bradshaw, J. L., Moss, S. A., Brereton, A. V., & Tonge, B. (2001). A deficit in shifting attention present in high-functioning autism but not Asperger’s disorder. Autism, 5(1), 67–80.CrossRefPubMedGoogle Scholar
  64. Rutter, M., Bailey, A., & Lord, C. (2003). Social Communication Questionnaire. Los Angeles, CA: Western Psychological Services.Google Scholar
  65. Sears, L. L., Vest, C., Mohamed, S., Bailey, J., Ranson, B. J., & Piven, J. (1999). An MRI study of the basal ganglia in autism. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 23(4), 613–624.CrossRefPubMedGoogle Scholar
  66. Shafritz, K. M., Dichter, G. S., Baranek, G. T., & Belger, A. (2008). The neural circuitry mediating shifts in behavioral response and cognitive set in autism. Biological Psychiatry, 63(10), 974–980.CrossRefPubMedCentralPubMedGoogle Scholar
  67. Solomon, M., Smith, A. C., Frank, M. J., Stanford, L., & Carter, C. S. (2011). Probabilistic reinforcement learning in adults with autism spectrum disorders. Autism Research, 4(2), 109–120.CrossRefPubMedGoogle Scholar
  68. South, M., Ozonoff, S., & McMahon, W. M. (2007). The relationship between executive functioning, central coherence, and repetitive behaviors in the high-functioning autism spectrum. Autism, 11(5), 437–451.CrossRefPubMedGoogle Scholar
  69. Takarae, Y., Minshew, N. J., Luna, B., Krisky, C. M., & Sweeney, J. A. (2004). Pursuit eye movement deficits in autism. Brain, 127, 2584–2594.CrossRefPubMedGoogle Scholar
  70. Takarae, Y., Minshew, N. J., Luna, B., & Sweeney, J. A. (2007). Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiatry Research, 156(2), 117–127.CrossRefPubMedCentralPubMedGoogle Scholar
  71. Turner, M. (1997). Towards an executive dysfunction account of repetitive behaviour in autism. In J. Russell (Ed.), Autism as an executive disorder (pp. 57–100). Oxford, NY: Oxford University Press.Google Scholar
  72. Van Eylen, L. V., Boets, B., Steyaert, J., Evers, K., Wagemans, J., & Noens, I. (2011). Cognitive flexibility in autism spectrum disorder: Explaining the inconsistencies? Research in Autism Spectrum Disorders, 5, 1390–1401.CrossRefGoogle Scholar
  73. Veenstra-VanderWeele, J., & Blakely, R. D. (2011). Networking in autism: Leveraging genetic, biomarker, and model system findings in the search for new treatments. Neuropsychopharmacology Reviews, 37, 196–212.CrossRefPubMedCentralPubMedGoogle Scholar
  74. Voelbel, G. T., Bates, M. E., Buckman, J. F., Pandina, G., & Hendren, R. L. (2006). Caudate nucleus volume and cognitive performance: Are they related in childhood psychopathology? Biological Psychiatry, 60(9), 942–950.CrossRefPubMedCentralPubMedGoogle Scholar
  75. Wechsler, D. (1999). Wechsler abbreviated scale of intelligence. San Antonio, TX: Pearson Clinical.Google Scholar
  76. Yerys, B. E., Wallace, G. L., Harrison, B., Celano, M. J., Giedd, J. N., & Kenworthy, L. E. (2009). Set-shifting in children with autism spectrum disorder: Reversal shifting deficits on the Intradimensional/Extradimensional Shift Test correlate with repetitive behaviors. Autism, 13(5), 523–538.PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Haylie L. Miller
    • 1
  • Michael E. Ragozzino
    • 2
  • Edwin H. Cook
    • 3
  • John A. Sweeney
    • 4
  • Matthew W. Mosconi
    • 4
  1. 1.Department of Physical TherapyUniversity of North Texas Health Science CenterFort WorthUSA
  2. 2.Department of PsychologyUniversity of Illinois at ChicagoChicagoUSA
  3. 3.Department of PsychiatryUniversity of Illinois at ChicagoChicagoUSA
  4. 4.Center for Autism and Developmental DisabilitiesUniversity of Texas Southwestern Medical CenterDallasUSA

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