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

  • M. W. Mosconi (a1), M. Kay (a1), A.-M. D'Cruz (a1), A. Seidenfeld (a1), S. Guter (a1), L. D. Stanford (a1) and J. A. Sweeney (a1)...
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.

Copyright
Corresponding author
*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)
References
Hide All
APA (2000). Diagnostic and Statistical Manual, 4th edn, text revision. American Psychiatric Association: Washington, DC.
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, 450461.
Boylan CB, Blue ME, Hohmann CF (2007). Modeling early cortical serotonergic deficits in autism. Behavioural Brain Research 176, 94108.
Christ SE, White DA, Brunstrom JE, Abrams RA (2003). Inhibitory control following perinatal brain injury. Neuropsychology 17, 171178.
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, 666669.
Cook EH Jr., Leventhal BL, Freedman DX (1988). Free serotonin in plasma: autistic children and their first-degree relatives. Biological Psychiatry 24, 488491.
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, 317.
DeLong GR, Teague LA, McSwain KM (1998). Effects of fluoxetine treatment in young children with idiopathic autism. Developmental Medicine and Child Neurology 40, 551562.
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, 27402754.
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, 387400.
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, 20392049.
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, 749765.
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, 31053112.
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.
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, 445460.
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, 205223.
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, 659685.
Luna B, Doll SK, Hegedus SJ, Minshew NJ, Sweeney JA (2007). Maturation of executive function in autism. Biological Psychiatry 61, 474481.
Luna B, Garver KE, Urban TA, Lazar NA, Sweeney JA (2004). Maturation of cognitive processes from late childhood to adulthood. Child Development 75, 13571372.
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, 17191726.
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, 17911798.
Maruff P, Purcell R, Tyler P, Pantellis C, Currie J (1999). Abnormalities of internally generated saccades in obsessive-compulsive disorder. Psychological Medicine 29, 13771385.
McEvoy RE, Rogers SJ, Pennington BF (1993). Executive function and social communication deficits in young autistic children. Journal of Child Psychology and Psychiatry 34, 563578.
Minshew NJ, Luna B, Sweeney JA (1999). Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology 52, 917922.
Moore ML, Eichner SF, Jones JR (2004). Treating functional impairment of autism with selective serotonin-reuptake inhibitors. Annals of Pharmacotherapy 38, 15151519.
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, 197205.
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, 343348.
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, 971986.
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, 831838.
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, 10961103.
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, 11631177.
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, 859868.
Schlag-Rey M, Amador N, Sanchez H, Schlag J (1997). Antisaccade performance predicted by neuronal activity in the supplementary eye field. Nature 390, 398401.
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, 716.
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, 437451.
Suvorov NF, Shuvaev VT, Voilokova NL, Chivileva OG, Shefer VI (1997). Corticostriatal mechanisms of behavior. Neuroscience and Behavioral Physiology 27, 653662.
Sweeney JA, Levy D, Harris MS (2002). Commentary: eye movement research with clinical populations. Progress in Brain Research 140, 507522.
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, 454468.
Takarae Y, Minshew NJ, Luna B, Sweeney JA (2004). Oculomotor abnormalities parallel cerebellar histopathology in autism. Journal of Neurology, Neurosurgery, and Psychiatry 75, 13591361.
Takarae Y, Minshew NJ, Luna B, Sweeney JA (2007). Atypical involvement of frontostriatal systems during sensorimotor control in autism. Psychiatry Research 156, 117127.
Taylor SF, Stern ER, Gehring WW (2007). Neural systems for error monitoring: recent findings and theoretical perspectives. Neuroscientist 13, 160172.
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, 24642478.
Tien AY, Pearlson GD, Machlin SR, Bylsma FW, Hoehn-Saric R (1992). Oculomotor performance in obsessive-compulsive disorder. American Journal of Psychiatry 149, 641646.
Turner M (1999). Annotation: Repetitive behaviour in autism: a review of psychological research. Journal of Child Psychology and Psychiatry 40, 839849.
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, 13211326.
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, 7583.
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Psychological Medicine
  • ISSN: 0033-2917
  • EISSN: 1469-8978
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