Hostname: page-component-8448b6f56d-gtxcr Total loading time: 0 Render date: 2024-04-19T01:11:02.534Z Has data issue: false hasContentIssue false
  • English
  • Français

Impaired inhibitory control is associated with higher-order repetitive behaviors in autism spectrum disorders

Published online by Cambridge University Press:  21 January 2009

M. W. Mosconi ,
M. Kay ,
A.-M. D'Cruz ,
A. Seidenfeld ,
S. Guter ,
L. D. Stanford  and
J. A. Sweeney
M. W. Mosconi
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
M. Kay
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
A.-M. D'Cruz
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
A. Seidenfeld
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
S. Guter
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
L. D. Stanford
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
J. A. Sweeney*
Affiliation:
Department of Psychiatry, Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
*
*Address for correspondence: Dr J. A. Sweeney, Center for Cognitive Medicine, 912 S. Wood St., MC 913, University of Illinois at Chicago, Chicago, IL 60612, USA. (Email: jsweeney@psych.uic.edu)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Impairments in executive cognitive control, including a reduced ability to inhibit prepotent responses, have been reported in autism spectrum disorders (ASD). These deficits may underlie patterns of repetitive behaviors associated with the disorder.

Method

Eighteen individuals with ASD and 15 age- and IQ-matched healthy individuals performed an antisaccade task and a visually guided saccade control task, each with gap and overlap conditions. Measures of repetitive behaviors were obtained using the Autism Diagnostic Inventory – Revised (ADI-R) and examined in relation to neurocognitive task performance.

Results

Individuals with an ASD showed increased rates of prosaccade errors (failures to inhibit prepotent responses) on the antisaccade task regardless of task condition (gap/overlap). Prosaccade error rates were associated with the level of higher-order (e.g. compulsions, preoccupations) but not sensorimotor repetitive behaviors in ASD.

Conclusions

Neurocognitive disturbances in voluntary behavioral control suggest that alterations in frontostriatal systems contribute to higher-order repetitive behaviors in ASD.

Keywords

Antisaccadeneurocognitionoculomotorprefrontal cortexstriatum
Type
Original Articles
Information
Psychological Medicine , Volume 39 , Issue 9 , September 2009 , pp. 1559 - 1566
Copyright
Copyright © 2009 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

APA (2000). Diagnostic and Statistical Manual, 4th edn, text revision. American Psychiatric Association: Washington, DC.Google Scholar
Bishop, SL, Richler, J, Cain, AC, Lord, C (2007). Predictors of perceived negative impact in mothers of children with autism spectrum disorder. American Journal of Mental Retardation 112, 450–461.CrossRefGoogle ScholarPubMed
Boylan, CB, Blue, ME, Hohmann, CF (2007). Modeling early cortical serotonergic deficits in autism. Behavioural Brain Research 176, 94–108.CrossRefGoogle ScholarPubMed
Christ, SE, White, DA, Brunstrom, JE, Abrams, RA (2003). Inhibitory control following perinatal brain injury. Neuropsychology 17, 171–178.CrossRefGoogle ScholarPubMed
Chugani, DC, Muzik, O, Rothermel, R, Behen, M, Chakraborty, P, Mangner, T, da Silva, EA, Chugani, HT (1997). Altered serotonin synthesis in the dentatothalamocortical pathway in autistic boys. Annals of Neurology 42, 666–669.CrossRefGoogle ScholarPubMed
Cook, EH Jr., Leventhal, BL, Freedman, DX (1988). Free serotonin in plasma: autistic children and their first-degree relatives. Biological Psychiatry 24, 488–491.CrossRefGoogle ScholarPubMed
Cuccaro, ML, Shao, Y, Grubber, J, Slifer, M, Wolpert, CM, Donnelly, SL, Abramson, RK, Ravan, SA, Wright, HH, DeLong, GR, Pericak-Vance, MA (2003). Factor analysis of restricted and repetitive behaviors in autism using the Autism Diagnostic Interview-R. Child Psychiatry and Human Development 34, 3–17.CrossRefGoogle ScholarPubMed
DeLong, GR, Teague, LA, McSwain, KM (1998). Effects of fluoxetine treatment in young children with idiopathic autism. Developmental Medicine and Child Neurology 40, 551–562.CrossRefGoogle ScholarPubMed
Everling, S, Dorris, MC, Klein, RM, Munoz, DP (1999). Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. Journal of Neuroscience 19, 2740–2754.CrossRefGoogle ScholarPubMed
Everling, S, Munoz, DP (2000). Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. Journal of Neuroscience 20, 387–400.CrossRefGoogle ScholarPubMed
Goldberg, MC, Lasker, AG, Zee, DS, Garth, E, Tien, A, Landa, RJ (2002). Deficits in the initiation of eye movements in the absence of a visual target in adolescents with high functioning autism. Neuropsychologia 40, 2039–2049.CrossRefGoogle ScholarPubMed
Johnston, K, Everling, S (2006). Neural activity in monkey prefrontal cortex is modulated by task context and behavioral instruction during delayed-match-to-sample and conditional prosaccade-antisaccade tasks. Journal of Cognitive Neuroscience 18, 749–765.CrossRefGoogle ScholarPubMed
Kelly, AM, Hester, R, Murphy, K, Javitt, DC, Foxe, JJ, Garavan, H (2004). Prefrontal-subcortical dissociations underlying inhibitory control revealed by event-related fMRI. European Journal of Neuroscience 19, 3105–3112.CrossRefGoogle ScholarPubMed
Liu, R, Sweeney, J, Minshew, N, Geier, C, Garver, K, Luna, B (2007). Developmental improvements in brain function supporting response inhibition from adolescence to adulthood in autism. Paper presented at the Annual Meeting of the Society for Neuroscience, San Diego, CA.Google Scholar
Lopez, BR, Lincoln, AJ, 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, 445–460.CrossRefGoogle ScholarPubMed
Lord, C, Risi, S, Lambrecht, L, Cook, EH Jr., Leventhal, BL, DiLavore, PC, Pickles, A, Rutter, M (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, 205–223.CrossRefGoogle ScholarPubMed
Lord, C, Rutter, M, Le Couteur, A (1994). Autism Diagnostic Interview – Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders 24, 659–685.CrossRefGoogle ScholarPubMed
Luna, B, Doll, SK, Hegedus, SJ, Minshew, NJ, Sweeney, JA (2007). Maturation of executive function in autism. Biological Psychiatry 61, 474–481.CrossRefGoogle ScholarPubMed
Luna, B, Garver, KE, Urban, TA, Lazar, NA, Sweeney, JA (2004). Maturation of cognitive processes from late childhood to adulthood. Child Development 75, 1357–1372.CrossRefGoogle ScholarPubMed
Manoach, DS, Lindgren, KA, Barton, JJS (2004). Deficient saccadic inhibition in Asperger's disorder and the social-emotional processing disorder. Journal of Neurology, Neurosurgery, and Psychiatry 75, 1719–1726.CrossRefGoogle ScholarPubMed
Manoach, DS, Thakkar, KN, Cain, MS, Polli, FE, Edelman, JA, Fischl, B, Barton, JJ (2007). Neural activity is modulated by trial history: a functional magnetic resonance imaging study of the effects of a previous antisaccade. Journal of Neuroscience 27, 1791–1798.CrossRefGoogle ScholarPubMed
Maruff, P, Purcell, R, Tyler, P, Pantellis, C, Currie, J (1999). Abnormalities of internally generated saccades in obsessive-compulsive disorder. Psychological Medicine 29, 1377–1385.CrossRefGoogle ScholarPubMed
McEvoy, RE, Rogers, SJ, Pennington, BF (1993). Executive function and social communication deficits in young autistic children. Journal of Child Psychology and Psychiatry 34, 563–578.CrossRefGoogle ScholarPubMed
Minshew, NJ, Luna, B, Sweeney, JA (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology 52, 917–922.CrossRefGoogle Scholar
Moore, ML, Eichner, SF, Jones, JR (2004). Treating functional impairment of autism with selective serotonin-reuptake inhibitors. Annals of Pharmacotherapy 38, 1515–1519.CrossRefGoogle ScholarPubMed
Moresco, RM, Pietra, L, Henin, M, Panzacchi, A, Locatelli, M, Bonaldi, L, Carinelli, A, Gobbo, C, Bellodi, L, Perani, D, Fazio, F (2007). Fluvoxamine treatment and D2 receptors: a PET study on OCD drug-naïve patients. Neuropsychopharmacology 32, 197–205.CrossRefGoogle Scholar
Owley, T, Walton, L, Salt, J, Guter, SJ Jr., Winnega, M, Leventhal, BL, Cook, EH Jr. (2005). An open-label trial of escitalopram in pervasive developmental disorders. Journal of the American Academy of Child and Adolescent Psychiatry 44, 343–348.CrossRefGoogle ScholarPubMed
Polli, FE, Barton, JJ, Thakkar, KN, Greve, DN, Goff, DC, Rauch, SL, Manoach, DS (2008). Reduced error-related activation in two anterior cingulate circuits is related to impaired performance in schizophrenia. Brain 131, 971–986.CrossRefGoogle Scholar
Rosenberg, DR, Averbach, DH, O'Hearn, KM, Seymour, AB, Birmaher, B, Sweeney, JA (1997). Oculomotor response inhibition abnormalities in pediatric obsessive-compulsive disorder. Archives of General Psychiatry 54, 831–838.CrossRefGoogle ScholarPubMed
Rosenberg, DR, McMaster, FP, Keshavan, MS, Fitzgerald, KD, Stewart, CM, Moore, GJ (2000). Decrease in caudate glutamatergic concentrations in pediatric obsessive-compulsive disorder patients taking paroxetine. Journal of the American Academy of Child and Adolescent Psychiatry 39, 1096–1103.CrossRefGoogle ScholarPubMed
Rubia, K, Smith, AB, Taylor, E, Brammer, M (2007). Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping 28, 1163–1177.CrossRefGoogle ScholarPubMed
Russell, J, Saltmarsh, R, Hill, E (1999). What do executive factors contribute to the failure on false belief tasks by children with autism? Journal of Child Psychology and Psychiatry 40, 859–868.CrossRefGoogle Scholar
Schlag-Rey, M, Amador, N, Sanchez, H, Schlag, J (1997). Antisaccade performance predicted by neuronal activity in the supplementary eye field. Nature 390, 398–401.CrossRefGoogle ScholarPubMed
Schmitz, N, Rubia, K, Daly, E, Smith, A, Williams, S, Murphy, DG (2006). Neural correlates of executive function in autistic spectrum disorders. Biological Psychiatry 59, 7–16.CrossRefGoogle ScholarPubMed
South, M, Ozonoff, S, McMahon, WM (2007). The relationship between executive functioning, central coherence, and repetitive behaviors in the high-functioning autism spectrum. Autism 11, 437–451.CrossRefGoogle ScholarPubMed
Suvorov, NF, Shuvaev, VT, Voilokova, NL, Chivileva, OG, Shefer, VI (1997). Corticostriatal mechanisms of behavior. Neuroscience and Behavioral Physiology 27, 653–662.CrossRefGoogle ScholarPubMed
Sweeney, JA, Levy, D, Harris, MS (2002). Commentary: eye movement research with clinical populations. Progress in Brain Research 140, 507–522.CrossRefGoogle ScholarPubMed
Sweeney, JA, Mintum, MA, Kwee, S, Wiseman, MB, Brown, DL, Rosenberg, DR, Carl, JR (1996). Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. Journal of Neurophysiology 75, 454–468.CrossRefGoogle ScholarPubMed
Takarae, Y, Minshew, NJ, Luna, B, Sweeney, JA (2004). Oculomotor abnormalities parallel cerebellar histopathology in autism. Journal of Neurology, Neurosurgery, and Psychiatry 75, 1359–1361.CrossRefGoogle ScholarPubMed
Takarae, Y, Minshew, NJ, Luna, B, Sweeney, JA (2007). Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiatry Research 156, 117–127.CrossRefGoogle ScholarPubMed
Taylor, SF, Stern, ER, Gehring, WW (2007). Neural systems for error monitoring: recent findings and theoretical perspectives. Neuroscientist 13, 160–172.CrossRefGoogle ScholarPubMed
Thakkar, KN, Polli, FE, Joseph, RM, Tuch, DS, Hadjikhani, N, Barton, JJS, Manoach, DS (2008). Response monitoring, repetitive behavior and anterior cingulate abnormalities in ASD. Brain 131, 2464–2478.CrossRefGoogle Scholar
Tien, AY, Pearlson, GD, Machlin, SR, Bylsma, FW, Hoehn-Saric, R (1992). Oculomotor performance in obsessive-compulsive disorder. American Journal of Psychiatry 149, 641–646.Google ScholarPubMed
Turner, M (1999). Annotation: Repetitive behaviour in autism: a review of psychological research. Journal of Child Psychology and Psychiatry 40, 839–849.CrossRefGoogle ScholarPubMed
van der Wee, NJ, Hardeman, HH, Ramsey, NF, Raemakers, M, Van Megen, HJ, Denys, DA, Westenberg, HG, Kahn, RS (2006). Saccadic abnormalities in psychotropic-naive obsessive-compulsive disorder without co-morbidity. Psychological Medicine 36, 1321–1326.CrossRefGoogle ScholarPubMed
Whitaker-Azmitia, PM (2005). Behavioral and cellular consequences of increasing serotonergic activity during brain development: a role in autism? International Journal of Developmental Neuroscience 23, 75–83.CrossRefGoogle ScholarPubMed